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

Shaqraa Musawi; Lise‐Marie Donnio; Zehui Zhao; Charlène Magnani; Phoebe Rassinoux; Olivier Binda; Jianbo Huang; Arnaud Jacquier; Laurent Coudert; Patrick Lomonte; Cécile Martinat; Laurent Schaeffer; Denis Mottet; Jocelyn Côté; Pierre‐Olivier Mari; Giuseppina Giglia‐Mari

doi:10.1038/s41467-023-42390-4

Molecular BiologyNature CommunicationsNov 15, 2023

Peer-reviewed journal article

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

Shaqraa Musawi iD, Lise‐Marie Donnio iD, Zehui Zhao iD, Charlène Magnani iD, Phoebe Rassinoux iD, Olivier Binda iD, Jianbo Huang iD, Arnaud Jacquier iD, Laurent Coudert iD, Patrick Lomonte iD, Cécile Martinat iD, Laurent Schaeffer iD, Denis Mottet iD, Jocelyn Côté iD, Pierre‐Olivier Mari iD, Giuseppina Giglia‐Mari iD

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Abstract

SMA is an autosomal recessive neuromuscular disease caused by mutations in the multifunctional protein SMN. Within the nucleus, SMN localizes to Cajal bodies (CBs), which have been shown to be 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. After genotoxic stress, RNAP1, Fibrillarin (FBL) and nucleolar DNA are exported to the periphery of the nucleolus and once DNA repair is fully completed the organization of the nucleolus is restored. We found that SMN is required for the restoration of the nucleolar structure after genotoxic stress. Unexpectedly, during DNA repair, SMN shuttles from the CBs to the nucleolus. This shuttling is important for nucleolar homeostasis and relies on the presence of Coilin and the activity of PRMT1.