IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-45788-w.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-45788-w
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-45788-w?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. 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.
    2. 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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Furqan Dar & Samuel R. Cohen & Diana M. Mitrea & Aaron H. Phillips & Gergely Nagy & Wellington C. Leite & Christopher B. Stanley & Jeong-Mo Choi & Richard W. Kriwacki & Rohit V. Pappu, 2024. "Biomolecular condensates form spatially inhomogeneous network fluids," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    2. Dinesh Sundaravadivelu Devarajan & Jiahui Wang & Beata Szała-Mendyk & Shiv Rekhi & Arash Nikoubashman & Young C. Kim & Jeetain Mittal, 2024. "Sequence-dependent material properties of biomolecular condensates and their relation to dilute phase conformations," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    3. Chongrui Zhang & Xufei Liu & Jiang Gong & Qiang Zhao, 2023. "Liquid sculpture and curing of bio-inspired polyelectrolyte aqueous two-phase systems," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    4. Miriam Linsenmeier & Maria Hondele & Fulvio Grigolato & Eleonora Secchi & Karsten Weis & Paolo Arosio, 2022. "Dynamic arrest and aging of biomolecular condensates are modulated by low-complexity domains, RNA and biochemical activity," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    5. Damian Wollny & Benjamin Vernot & Jie Wang & Maria Hondele & Aram Safrastyan & Franziska Aron & Julia Micheel & Zhisong He & Anthony Hyman & Karsten Weis & J. Gray Camp & T.‐Y. Dora Tang & Barbara Tre, 2022. "Characterization of RNA content in individual phase-separated coacervate microdroplets," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    6. Ibraheem Alshareedah & Mahdi Muhammad Moosa & Matthew Pham & Davit A. Potoyan & Priya R. Banerjee, 2021. "Programmable viscoelasticity in protein-RNA condensates with disordered sticker-spacer polypeptides," Nature Communications, Nature, vol. 12(1), pages 1-14, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45788-w. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.