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The dual life of disordered lysine-rich domains of snoRNPs in rRNA modification and nucleolar compaction

Author

Listed:
  • Carine Dominique

    (UPS)

  • Nana Kadidia Maiga

    (UPS)

  • Alfonso Méndez-Godoy

    (University of Fribourg)

  • Benjamin Pillet

    (University of Fribourg)

  • Hussein Hamze

    (UPS)

  • Isabelle Léger-Silvestre

    (UPS)

  • Yves Henry

    (UPS)

  • Virginie Marchand

    (UAR2008 IBSLor/UMR7365 IMoPA)

  • Valdir Gomes Neto

    (University of São Paulo)

  • Christophe Dez

    (UPS)

  • Yuri Motorin

    (UAR2008 IBSLor/UMR7365 IMoPA)

  • Dieter Kressler

    (University of Fribourg)

  • Olivier Gadal

    (UPS)

  • Anthony K. Henras

    (UPS)

  • Benjamin Albert

    (UPS)

Abstract

Intrinsically disordered regions (IDRs) are highly enriched in the nucleolar proteome but their physiological role in ribosome assembly remains poorly understood. Our study reveals the functional plasticity of the extremely abundant lysine-rich IDRs of small nucleolar ribonucleoprotein particles (snoRNPs) from protists to mammalian cells. We show in Saccharomyces cerevisiae that the electrostatic properties of this lysine-rich IDR, the KKE/D domain, promote snoRNP accumulation in the vicinity of nascent rRNAs, facilitating their modification. Under stress conditions reducing the rate of ribosome assembly, they are essential for nucleolar compaction and sequestration of key early-acting ribosome biogenesis factors, including RNA polymerase I, owing to their self-interaction capacity in a latent, non-rRNA-associated state. We propose that such functional plasticity of these lysine-rich IDRs may represent an ancestral eukaryotic regulatory mechanism, explaining how nucleolar morphology is continuously adapted to rRNA production levels.

Suggested Citation

  • Carine Dominique & Nana Kadidia Maiga & Alfonso Méndez-Godoy & Benjamin Pillet & Hussein Hamze & Isabelle Léger-Silvestre & Yves Henry & Virginie Marchand & Valdir Gomes Neto & Christophe Dez & Yuri M, 2024. "The dual life of disordered lysine-rich domains of snoRNPs in rRNA modification and nucleolar compaction," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-53805-1
    DOI: 10.1038/s41467-024-53805-1
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    1. Joshua A. Riback & Lian Zhu & Mylene C. Ferrolino & Michele Tolbert & Diana M. Mitrea & David W. Sanders & Ming-Tzo Wei & Richard W. Kriwacki & Clifford P. Brangwynne, 2020. "Composition-dependent thermodynamics of intracellular phase separation," Nature, Nature, vol. 581(7807), pages 209-214, May.
    2. Diana M. Mitrea & Jaclyn A. Cika & Christopher B. Stanley & Amanda Nourse & Paulo L. Onuchic & Priya R. Banerjee & Aaron H. Phillips & Cheon-Gil Park & Ashok A. Deniz & Richard W. Kriwacki, 2018. "Self-interaction of NPM1 modulates multiple mechanisms of liquid–liquid phase separation," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    3. Won-Ki Huh & James V. Falvo & Luke C. Gerke & Adam S. Carroll & Russell W. Howson & Jonathan S. Weissman & Erin K. O'Shea, 2003. "Global analysis of protein localization in budding yeast," Nature, Nature, vol. 425(6959), pages 686-691, October.
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