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Nucleolar reorganization after cellular stress is orchestrated by SMN shuttling between nuclear compartments

Author

Listed:
  • Shaqraa Musawi

    (CNRS UMR 5261, INSERM U1315, Université Claude Bernard Lyon 1
    Jazan University)

  • Lise-Marie Donnio

    (CNRS UMR 5261, INSERM U1315, Université Claude Bernard Lyon 1)

  • Zehui Zhao

    (CNRS UMR 5261, INSERM U1315, Université Claude Bernard Lyon 1)

  • Charlène Magnani

    (CNRS UMR 5261, INSERM U1315, Université Claude Bernard Lyon 1)

  • Phoebe Rassinoux

    (CNRS UMR 5261, INSERM U1315, Université Claude Bernard Lyon 1)

  • Olivier Binda

    (CNRS UMR 5261, INSERM U1315, Université Claude Bernard Lyon 1
    University of Ottawa)

  • Jianbo Huang

    (CNRS UMR 5261, INSERM U1315, Université Claude Bernard Lyon 1)

  • Arnaud Jacquier

    (CNRS UMR 5261, INSERM U1315, Université Claude Bernard Lyon 1)

  • Laurent Coudert

    (CNRS UMR 5261, INSERM U1315, Université Claude Bernard Lyon 1)

  • Patrick Lomonte

    (CNRS UMR 5261, INSERM U1315, Université Claude Bernard Lyon 1)

  • Cécile Martinat

    (INSERM/UEPS UMR 861, Paris Saclay Université, I-STEM)

  • Laurent Schaeffer

    (CNRS UMR 5261, INSERM U1315, Université Claude Bernard Lyon 1)

  • Denis Mottet

    (University of Liege)

  • Jocelyn Côté

    (University of Ottawa)

  • Pierre-Olivier Mari

    (CNRS UMR 5261, INSERM U1315, Université Claude Bernard Lyon 1)

  • Giuseppina Giglia-Mari

    (CNRS UMR 5261, INSERM U1315, Université Claude Bernard Lyon 1)

Abstract

Spinal muscular atrophy is an autosomal recessive neuromuscular disease caused by mutations in the multifunctional protein Survival of Motor Neuron, or SMN. Within the nucleus, SMN localizes to Cajal bodies, which are associated with nucleoli, nuclear organelles dedicated to the first steps of ribosome biogenesis. The highly organized structure of the nucleolus can be dynamically altered by genotoxic agents. RNAP1, Fibrillarin, and nucleolar DNA are exported to the periphery of the nucleolus after genotoxic stress and, once DNA repair is fully completed, the organization of the nucleolus is restored. We find that SMN is required for the restoration of the nucleolar structure after genotoxic stress. During DNA repair, SMN shuttles from the Cajal bodies to the nucleolus. This shuttling is important for nucleolar homeostasis and relies on the presence of Coilin and the activity of PRMT1.

Suggested Citation

  • Shaqraa Musawi & Lise-Marie Donnio & Zehui Zhao & Charlène Magnani & Phoebe Rassinoux & Olivier Binda & Jianbo Huang & Arnaud Jacquier & Laurent Coudert & Patrick Lomonte & Cécile Martinat & Laurent S, 2023. "Nucleolar reorganization after cellular stress is orchestrated by SMN shuttling between nuclear compartments," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42390-4
    DOI: 10.1038/s41467-023-42390-4
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    References listed on IDEAS

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    1. Namrata Kumar & Arjan F. Theil & Vera Roginskaya & Yasmin Ali & Michael Calderon & Simon C. Watkins & Ryan P. Barnes & Patricia L. Opresko & Alex Pines & Hannes Lans & Wim Vermeulen & Bennett Houten, 2022. "Global and transcription-coupled repair of 8-oxoG is initiated by nucleotide excision repair proteins," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    2. Dorothy Yanling Zhao & Gerald Gish & Ulrich Braunschweig & Yue Li & Zuyao Ni & Frank W. Schmitges & Guoqing Zhong & Ke Liu & Weiguo Li & Jason Moffat & Masoud Vedadi & Jinrong Min & Tony J. Pawson & B, 2016. "SMN and symmetric arginine dimethylation of RNA polymerase II C-terminal domain control termination," Nature, Nature, vol. 529(7584), pages 48-53, January.
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    1. Negin Khosraviani & V. Talya Yerlici & Jonathan St-Germain & Yi Yang Hou & Shi Bo Cao & Carla Ghali & Michael Bokros & Rehna Krishnan & Razqallah Hakem & Stephen Lee & Brian Raught & Karim Mekhail, 2024. "Nucleolar Pol II interactome reveals TBPL1, PAF1, and Pol I at intergenic rDNA drive rRNA biogenesis," Nature Communications, Nature, vol. 15(1), pages 1-17, December.

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