IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v16y2025i1d10.1038_s41467-025-57592-1.html
   My bibliography  Save this article

The DEAD-box helicase eIF4A1/2 acts as RNA chaperone during mitotic exit enabling chromatin decondensation

Author

Listed:
  • Ramona Jühlen

    (RWTH Aachen University)

  • Sabine C. Wiesmann

    (RWTH Aachen University)

  • Anja Scheufen

    (RWTH Aachen University)

  • Thilo Stausberg

    (RWTH Aachen University)

  • Isabel Braun

    (RWTH Aachen University)

  • Chantal Strobel

    (RWTH Aachen University)

  • Carmen Llera-Brandt

    (RWTH Aachen University)

  • Sabrina Rappold

    (RWTH Aachen University)

  • Rabia Suluyayla

    (RWTH Aachen University)

  • Marianna Tatarek-Nossol

    (RWTH Aachen University)

  • Birgitt Lennartz

    (RWTH Aachen University)

  • Hongqi Lue

    (RWTH Aachen University)

  • Maximilian W. G. Schneider

    (RWTH Aachen University)

  • Juan-Felipe Perez-Correa

    (RWTH Aachen University)

  • Daniel Moreno-Andrés

    (RWTH Aachen University)

  • Wolfram Antonin

    (RWTH Aachen University)

Abstract

During mitosis, chromosomes condense and decondense to segregate faithfully and undamaged. The exact molecular mechanisms are not well understood. We identify the DEAD-box helicase eIF4A1/2 as a critical factor in this process. In a cell-free condensation assay eIF4A1/2 is crucial for this process, relying on its RNA-binding ability but not its ATPase activity. Reducing eIF4A1/2 levels in cells consistently slows down chromatin decondensation during nuclear reformation. Conversely, increasing eIF4A1/2 concentration on mitotic chromosomes accelerates their decondensation. The absence of eIF4A1/2 affects the perichromatin layer, which surrounds the chromosomes during mitosis and consists of RNA and mainly nucleolar proteins. In vitro, eIF4A1/2 acts as an RNA chaperone, dissociating biomolecular condensates of RNA and perichromatin proteins. During mitosis, the chaperone activity of eIF4A1/2 is required to regulate the composition and fluidity of the perichromatin layer, which is crucial for the dynamic reorganization of chromatin as cells exit mitosis.

Suggested Citation

  • Ramona Jühlen & Sabine C. Wiesmann & Anja Scheufen & Thilo Stausberg & Isabel Braun & Chantal Strobel & Carmen Llera-Brandt & Sabrina Rappold & Rabia Suluyayla & Marianna Tatarek-Nossol & Birgitt Lenn, 2025. "The DEAD-box helicase eIF4A1/2 acts as RNA chaperone during mitotic exit enabling chromatin decondensation," Nature Communications, Nature, vol. 16(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-57592-1
    DOI: 10.1038/s41467-025-57592-1
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-025-57592-1
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-025-57592-1?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. Sara Cuylen-Haering & Mina Petrovic & Alberto Hernandez-Armendariz & Maximilian W. G. Schneider & Matthias Samwer & Claudia Blaukopf & Liam J. Holt & Daniel W. Gerlich, 2020. "Chromosome clustering by Ki-67 excludes cytoplasm during nuclear assembly," Nature, Nature, vol. 587(7833), pages 285-290, November.
    2. Sara Cuylen & Claudia Blaukopf & Antonio Z. Politi & Thomas Müller-Reichert & Beate Neumann & Ina Poser & Jan Ellenberg & Anthony A. Hyman & Daniel W. Gerlich, 2016. "Ki-67 acts as a biological surfactant to disperse mitotic chromosomes," Nature, Nature, vol. 535(7611), pages 308-312, July.
    3. Kristijan Ramadan & Roland Bruderer & Fabio M. Spiga & Oliver Popp & Tina Baur & Monica Gotta & Hemmo H. Meyer, 2007. "Cdc48/p97 promotes reformation of the nucleus by extracting the kinase Aurora B from chromatin," Nature, Nature, vol. 450(7173), pages 1258-1262, December.
    4. Maria Hondele & Ruchika Sachdev & Stephanie Heinrich & Juan Wang & Pascal Vallotton & Beatriz M. A. Fontoura & Karsten Weis, 2019. "DEAD-box ATPases are global regulators of phase-separated organelles," Nature, Nature, vol. 573(7772), pages 144-148, September.
    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. Juliette Ferrand & Juliette Dabin & Odile Chevallier & Matteo Kane-Charvin & Ariana Kupai & Joel Hrit & Scott B. Rothbart & Sophie E. Polo, 2025. "Mitotic chromatin marking governs the segregation of DNA damage," Nature Communications, Nature, vol. 16(1), pages 1-12, December.
    2. Sheung Chun Ng & Abin Biswas & Trevor Huyton & Jürgen Schünemann & Simone Reber & Dirk Görlich, 2023. "Barrier properties of Nup98 FG phases ruled by FG motif identity and inter-FG spacer length," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    3. Chun Hei Li & Noortje Kersten & Nazmiye Özkan & Dan T. M. Nguyen & Max Koppers & Harm Post & Maarten Altelaar & Ginny G. Farias, 2024. "Spatiotemporal proteomics reveals the biosynthetic lysosomal membrane protein interactome in neurons," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    4. Bing-Ze Yang & Mei-Yin Liu & Kuan-Lin Chiu & Yuh-Ling Chien & Ching-An Cheng & Yu-Lin Chen & Li-Yu Tsui & Keng-Ru Lin & Hsueh-Ping Catherine Chu & Ching-Shyi Peter Wu, 2024. "DHX9 SUMOylation is required for the suppression of R-loop-associated genome instability," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    5. Henrik M. Hammarén & Eva-Maria Geissen & Clement M. Potel & Martin Beck & Mikhail M. Savitski, 2022. "Protein-Peptide Turnover Profiling reveals the order of PTM addition and removal during protein maturation," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    6. Xianle Shi & Yanjing Li & Hongwei Zhou & Xiukun Hou & Jihong Yang & Vikas Malik & Francesco Faiola & Junjun Ding & Xichen Bao & Miha Modic & Weiyu Zhang & Lingyi Chen & Syed Raza Mahmood & Effie Apost, 2024. "DDX18 coordinates nucleolus phase separation and nuclear organization to control the pluripotency of human embryonic stem cells," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    7. Johanna Luige & Alexandros Armaos & Gian Gaetano Tartaglia & Ulf Andersson Vang Ørom, 2024. "Predicting nuclear G-quadruplex RNA-binding proteins with roles in transcription and phase separation," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    8. Etienne Jambon-Puillet & Andrea Testa & Charlotta Lorenz & Robert W. Style & Aleksander A. Rebane & Eric R. Dufresne, 2024. "Phase-separated droplets swim to their dissolution," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    9. Karl E. Bauer & Niklas Bargenda & Rico Schieweck & Christin Illig & Inmaculada Segura & Max Harner & Michael A. Kiebler, 2022. "RNA supply drives physiological granule assembly in neurons," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    10. Aidan M. Fenix & Yuichiro Miyaoka & Alessandro Bertero & Steven M. Blue & Matthew J. Spindler & Kenneth K. B. Tan & Juan A. Perez-Bermejo & Amanda H. Chan & Steven J. Mayerl & Trieu D. Nguyen & Caitli, 2021. "Gain-of-function cardiomyopathic mutations in RBM20 rewire splicing regulation and re-distribute ribonucleoprotein granules within processing bodies," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    11. Zhaowei Yu & Qi Wang & Qichen Zhang & Yawen Tian & Guo Yan & Jidong Zhu & Guangya Zhu & Yong Zhang, 2024. "Decoding the genomic landscape of chromatin-associated biomolecular condensates," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    12. 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.
    13. Lior Aroeti & Netanel Elbaz & Raya Faigenbaum-Romm & Oren Yakovian & Yael Altuvia & Liron Argaman & Naama Katsowich & Michal Bejerano-Sagie & Miriam Ravins & Hanah Margalit & Sigal Ben-Yehuda & Ilan R, 2025. "Formation of a membraneless compartment regulates bacterial virulence," Nature Communications, Nature, vol. 16(1), pages 1-14, December.
    14. Ebru Aydin & Silke Schreiner & Jacqueline Böhme & Birte Keil & Jan Weber & Bojan Žunar & Timo Glatter & Cornelia Kilchert, 2024. "DEAD-box ATPase Dbp2 is the key enzyme in an mRNP assembly checkpoint at the 3’-end of genes and involved in the recycling of cleavage factors," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    15. Ravi Chawla & Jenna K. A. Tom & Tumara Boyd & Nicholas H. Tu & Tanxi Bai & Danielle A. Grotjahn & Donghyun Park & Ashok A. Deniz & Lisa R. Racki, 2024. "Reentrant DNA shells tune polyphosphate condensate size," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    16. Marcos Gil-Garcia & Ana I. Benítez-Mateos & Marcell Papp & Florence Stoffel & Chiara Morelli & Karl Normak & Katarzyna Makasewicz & Lenka Faltova & Francesca Paradisi & Paolo Arosio, 2024. "Local environment in biomolecular condensates modulates enzymatic activity across length scales," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    17. Kayo Hibino & Yuji Sakai & Sachiko Tamura & Masatoshi Takagi & Katsuhiko Minami & Toyoaki Natsume & Masa A. Shimazoe & Masato T. Kanemaki & Naoko Imamoto & Kazuhiro Maeshima, 2024. "Single-nucleosome imaging unveils that condensins and nucleosome–nucleosome interactions differentially constrain chromatin to organize mitotic chromosomes," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    18. 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.
    19. Liguo Wang & Christopher Brasnett & Luís Borges-Araújo & Paulo C. T. Souza & Siewert J. Marrink, 2025. "Martini3-IDP: improved Martini 3 force field for disordered proteins," Nature Communications, Nature, vol. 16(1), pages 1-14, December.
    20. Michael C. Owens & Hui Shen & Amber Yanas & Maria Saraí Mendoza-Figueroa & Ellen Lavorando & Xiaoyu Wei & Him Shweta & Hsin-Yao Tang & Yale E. Goldman & Kathy Fange Liu, 2024. "Specific catalytically impaired DDX3X mutants form sexually dimorphic hollow condensates," Nature Communications, Nature, vol. 15(1), pages 1-17, 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:16:y:2025:i:1:d:10.1038_s41467-025-57592-1. 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.