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Large dynamics of a phase separating arginine-glycine-rich domain revealed via nuclear and electron spins

Author

Listed:
  • Giuseppe Sicoli

    (University of Lille, LASIRE)

  • Daniel Sieme

    (Max Planck Institute for Multidisciplinary Sciences)

  • Kerstin Overkamp

    (Max Planck Institute for Multidisciplinary Sciences)

  • Mahdi Khalil

    (University of Lille, LASIRE)

  • Robin Backer

    (Heinrich Heine University (HHU) Düsseldorf, Faculty of Mathematics and Natural Sciences, Institute of Physical Biology)

  • Christian Griesinger

    (Max Planck Institute for Multidisciplinary Sciences)

  • Dieter Willbold

    (Heinrich Heine University (HHU) Düsseldorf, Faculty of Mathematics and Natural Sciences, Institute of Physical Biology
    IBI-7: Structural Biochemistry, Forschungszentrum Jülich)

  • Nasrollah Rezaei-Ghaleh

    (Heinrich Heine University (HHU) Düsseldorf, Faculty of Mathematics and Natural Sciences, Institute of Physical Biology
    IBI-7: Structural Biochemistry, Forschungszentrum Jülich)

Abstract

Liquid-liquid phase separation is the key process underlying formation of membrane-less compartments in cells. A highly dynamic cellular body with rapid component exchange is Cajal body (CB), which supports the extensive compositional dynamics of the RNA splicing machinery, spliceosome. Here, we select an arginine-glycine (RG)-rich segment of coilin, the major component of CB, establish its RNA-induced phase separation, and through combined use of nuclear magnetic resonance (NMR) and electron paramagnetic resonance (EPR) probes, interrogate its dynamics within the crowded interior of formed droplets. Taking advantage of glycine-based singlet-states, we show that glycines retain a large level of sub-nanoseconds dynamics inside the coilin droplets. Furthermore, the continuous-wave (CW) and electron-electron dipolar (PELDOR) and electron-nucleus hyperfine coupling EPR data (HYSCORE) support the RNA-induced formation of dynamic coilin droplets with high coilin peptide concentrations. The combined NMR and EPR data reveal the high dynamics of the RG-rich coilin within droplets and suggest its potential role in the large dynamics of CBs.

Suggested Citation

  • Giuseppe Sicoli & Daniel Sieme & Kerstin Overkamp & Mahdi Khalil & Robin Backer & Christian Griesinger & Dieter Willbold & Nasrollah Rezaei-Ghaleh, 2024. "Large dynamics of a phase separating arginine-glycine-rich domain revealed via nuclear and electron spins," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45788-w
    DOI: 10.1038/s41467-024-45788-w
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    References listed on IDEAS

    as
    1. Archishman Ghosh & Divya Kota & Huan-Xiang Zhou, 2021. "Shear relaxation governs fusion dynamics of biomolecular condensates," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    2. Tina Ukmar-Godec & Saskia Hutten & Matthew P. Grieshop & Nasrollah Rezaei-Ghaleh & Maria-Sol Cima-Omori & Jacek Biernat & Eckhard Mandelkow & Johannes Söding & Dorothee Dormann & Markus Zweckstetter, 2019. "Lysine/RNA-interactions drive and regulate biomolecular condensation," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
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