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RSL24D1 sustains steady-state ribosome biogenesis and pluripotency translational programs in embryonic stem cells

Author

Listed:
  • Sébastien Durand

    (Université Claude Bernard Lyon I, Centre Léon Bérard
    Institut Convergence Plascan
    Labex Dev2Can)

  • Marion Bruelle

    (Université Claude Bernard Lyon I, Centre Léon Bérard)

  • Fleur Bourdelais

    (Université Claude Bernard Lyon I, Centre Léon Bérard
    Institut Convergence Plascan
    Labex Dev2Can
    Inovarion)

  • Bigitha Bennychen

    (University of Ottawa
    National Research Council Canada)

  • Juliana Blin-Gonthier

    (Laboratoire de Biologie et de Modélisation de la Cellule, ENS de Lyon, CNRS UMR 5239, Inserm U1293)

  • Caroline Isaac

    (Université Claude Bernard Lyon I, Centre Léon Bérard
    Institut Convergence Plascan
    Labex Dev2Can)

  • Aurélia Huyghe

    (Université Claude Bernard Lyon I, Centre Léon Bérard
    Institut Convergence Plascan
    Labex Dev2Can
    Equipe labellisée la Ligue contre le cancer)

  • Sylvie Martel

    (Université Claude Bernard Lyon I, Centre Léon Bérard
    Institut Convergence Plascan)

  • Antoine Seyve

    (Université Claude Bernard Lyon I, Centre Léon Bérard
    Institut Convergence Plascan
    Hospices Civils de Lyon)

  • Christophe Vanbelle

    (Université Claude Bernard Lyon I, Centre Léon Bérard
    Institut Convergence Plascan)

  • Annie Adrait

    (University Grenoble Alpes, INSERM, CEA, UA13 BGE, CNRS, CEA, FR2048, 38000)

  • Yohann Couté

    (University Grenoble Alpes, INSERM, CEA, UA13 BGE, CNRS, CEA, FR2048, 38000)

  • David Meyronet

    (Université Claude Bernard Lyon I, Centre Léon Bérard
    Institut Convergence Plascan
    Institut de Pathologie Est, Hospices Civils de Lyon)

  • Frédéric Catez

    (Université Claude Bernard Lyon I, Centre Léon Bérard
    Institut Convergence Plascan
    Labex Dev2Can)

  • Jean-Jacques Diaz

    (Université Claude Bernard Lyon I, Centre Léon Bérard
    Institut Convergence Plascan
    Labex Dev2Can)

  • Fabrice Lavial

    (Université Claude Bernard Lyon I, Centre Léon Bérard
    Institut Convergence Plascan
    Labex Dev2Can
    Equipe labellisée la Ligue contre le cancer)

  • Emiliano P. Ricci

    (Laboratoire de Biologie et de Modélisation de la Cellule, ENS de Lyon, CNRS UMR 5239, Inserm U1293)

  • François Ducray

    (Université Claude Bernard Lyon I, Centre Léon Bérard
    Institut Convergence Plascan
    Hospices Civils de Lyon)

  • Mathieu Gabut

    (Université Claude Bernard Lyon I, Centre Léon Bérard
    Institut Convergence Plascan)

Abstract

Embryonic stem cell (ESC) fate decisions are regulated by a complex circuitry that coordinates gene expression at multiple levels from chromatin to mRNA processing. Recently, ribosome biogenesis and translation have emerged as key pathways that efficiently control stem cell homeostasis, yet the underlying molecular mechanisms remain largely unknown. Here, we identified RSL24D1 as highly expressed in both mouse and human pluripotent stem cells. RSL24D1 is associated with nuclear pre-ribosomes and is required for the biogenesis of 60S subunits in mouse ESCs. Interestingly, RSL24D1 depletion significantly impairs global translation, particularly of key pluripotency factors and of components from the Polycomb Repressive Complex 2 (PRC2). While having a moderate impact on differentiation, RSL24D1 depletion significantly alters ESC self-renewal and lineage commitment choices. Altogether, these results demonstrate that RSL24D1-dependant ribosome biogenesis is both required to sustain the expression of pluripotent transcriptional programs and to silence PRC2-regulated developmental programs, which concertedly dictate ESC homeostasis.

Suggested Citation

  • Sébastien Durand & Marion Bruelle & Fleur Bourdelais & Bigitha Bennychen & Juliana Blin-Gonthier & Caroline Isaac & Aurélia Huyghe & Sylvie Martel & Antoine Seyve & Christophe Vanbelle & Annie Adrait , 2023. "RSL24D1 sustains steady-state ribosome biogenesis and pluripotency translational programs in embryonic stem cells," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36037-7
    DOI: 10.1038/s41467-023-36037-7
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    References listed on IDEAS

    as
    1. Yi Zhou & Sharmishtha Musalgaonkar & Arlen W. Johnson & David W. Taylor, 2019. "Tightly-orchestrated rearrangements govern catalytic center assembly of the ribosome," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    2. Hongwei Chen & Irène Aksoy & Fabrice Gonnot & Pierre Osteil & Maxime Aubry & Claire Hamela & Cloé Rognard & Arnaud Hochard & Sophie Voisin & Emeline Fontaine & Magali Mure & Marielle Afanassieff & Elo, 2015. "Reinforcement of STAT3 activity reprogrammes human embryonic stem cells to naive-like pluripotency," Nature Communications, Nature, vol. 6(1), pages 1-17, November.
    3. Alejandro De Los Angeles & Francesco Ferrari & Ruibin Xi & Yuko Fujiwara & Nissim Benvenisty & Hongkui Deng & Konrad Hochedlinger & Rudolf Jaenisch & Soohyun Lee & Harry G. Leitch & M. William Lensch , 2015. "Hallmarks of pluripotency," Nature, Nature, vol. 525(7570), pages 469-478, September.
    4. Akshay K. Ahuja & Karolina Jodkowska & Federico Teloni & Anna H. Bizard & Ralph Zellweger & Raquel Herrador & Sagrario Ortega & Ian D. Hickson & Matthias Altmeyer & Juan Mendez & Massimo Lopes, 2016. "A short G1 phase imposes constitutive replication stress and fork remodelling in mouse embryonic stem cells," Nature Communications, Nature, vol. 7(1), pages 1-11, April.
    5. Stefan Semrau & Johanna E. Goldmann & Magali Soumillon & Tarjei S. Mikkelsen & Rudolf Jaenisch & Alexander van Oudenaarden, 2017. "Dynamics of lineage commitment revealed by single-cell transcriptomics of differentiating embryonic stem cells," Nature Communications, Nature, vol. 8(1), pages 1-16, December.
    6. Kotaro Fujii & Zhen Shi & Olena Zhulyn & Nicolas Denans & Maria Barna, 2017. "Pervasive translational regulation of the cell signalling circuitry underlies mammalian development," Nature Communications, Nature, vol. 8(1), pages 1-13, April.
    7. Duygu Ozmadenci & Olivier Féraud & Suzy Markossian & Elsa Kress & Benjamin Ducarouge & Benjamin Gibert & Jian Ge & Isabelle Durand & Nicolas Gadot & Michela Plateroti & Annelise Bennaceur-Griscelli & , 2015. "Netrin-1 regulates somatic cell reprogramming and pluripotency maintenance," Nature Communications, Nature, vol. 6(1), pages 1-11, November.
    8. Chet H. Loh & Siebe Genesen & Matteo Perino & Magnus R. Bark & Gert Jan C. Veenstra, 2021. "Loss of PRC2 subunits primes lineage choice during exit of pluripotency," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    9. Björn Schwanhäusser & Dorothea Busse & Na Li & Gunnar Dittmar & Johannes Schuchhardt & Jana Wolf & Wei Chen & Matthias Selbach, 2011. "Global quantification of mammalian gene expression control," Nature, Nature, vol. 473(7347), pages 337-342, May.
    10. Rong Lu & Florian Markowetz & Richard D. Unwin & Jeffrey T. Leek & Edoardo M. Airoldi & Ben D. MacArthur & Alexander Lachmann & Roye Rozov & Avi Ma’ayan & Laurie A. Boyer & Olga G. Troyanskaya & Antho, 2009. "Systems-level dynamic analyses of fate change in murine embryonic stem cells," Nature, Nature, vol. 462(7271), pages 358-362, November.
    11. Elisa Lavarone & Caterina M. Barbieri & Diego Pasini, 2019. "Dissecting the role of H3K27 acetylation and methylation in PRC2 mediated control of cellular identity," Nature Communications, Nature, vol. 10(1), pages 1-16, December.
    12. Xiaomeng Liang & Mei-Qing Zuo & Yunyang Zhang & Ningning Li & Chengying Ma & Meng-Qiu Dong & Ning Gao, 2020. "Structural snapshots of human pre-60S ribosomal particles before and after nuclear export," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
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    1. Pui Pik Law & Liudmila A. Mikheeva & Francisco Rodriguez-Algarra & Fredrika Asenius & Maria Gregori & Robert A. E. Seaborne & Selin Yildizoglu & James R. C. Miller & Hemanth Tummala & Robin Mesnage & , 2024. "Ribosomal DNA copy number is associated with body mass in humans and other mammals," Nature Communications, Nature, vol. 15(1), pages 1-11, December.

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