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An atlas of RNA-dependent proteins in cell division reveals the riboregulation of mitotic protein-protein interactions

Author

Listed:
  • Varshni Rajagopal

    (German Cancer Research Center (DKFZ))

  • Jeanette Seiler

    (German Cancer Research Center (DKFZ))

  • Isha Nasa

    (Geisel School of Medicine at Dartmouth
    Geisel School of Medicine at Dartmouth)

  • Simona Cantarella

    (German Cancer Research Center (DKFZ))

  • Jana Theiss

    (German Cancer Research Center (DKFZ))

  • Franziska Herget

    (German Cancer Research Center (DKFZ))

  • Bianca Kaifer

    (German Cancer Research Center (DKFZ))

  • Melina Klostermann

    (Buchmann Institute for Molecular Life Sciences
    University of Würzburg)

  • Rainer Will

    (German Cancer Research Center (DKFZ))

  • Martin Schneider

    (German Cancer Research Center (DKFZ))

  • Dominic Helm

    (German Cancer Research Center (DKFZ))

  • Julian König

    (Institute of Molecular Biology (IMB)
    University of Würzburg)

  • Kathi Zarnack

    (Buchmann Institute for Molecular Life Sciences
    University of Würzburg)

  • Sven Diederichs

    (University of Freiburg
    a partnership between DKFZ and University Medical Center Freiburg)

  • Arminja N. Kettenbach

    (Geisel School of Medicine at Dartmouth
    Geisel School of Medicine at Dartmouth)

  • Maïwen Caudron-Herger

    (German Cancer Research Center (DKFZ))

Abstract

Ribonucleoprotein complexes are dynamic assemblies of RNA with RNA-binding proteins, which modulate the fate of RNA. Inversely, RNA riboregulates the interactions and functions of the associated proteins. Dysregulation of ribonucleoprotein functions is linked to diseases such as cancer and neurological disorders. In dividing cells, RNA and RNA-binding proteins are present in mitotic structures, but their impact on cell division remains unclear. By applying the proteome-wide R-DeeP strategy to cells synchronized in mitosis versus interphase integrated with the RBP2GO knowledge, we provided an atlas of RNA-dependent proteins in cell division, accessible at R-DeeP3.dkfz.de. We uncovered AURKA, KIFC1 and TPX2 as unconventional RNA-binding proteins. KIFC1 was identified as a new substrate of AURKA, and new TPX2-interacting protein. Their pair-wise interactions were RNA dependent. In addition, RNA stimulated AURKA kinase activity and stabilized its conformation. In this work, we highlighted riboregulation of major mitotic factors as an additional complexity level of cell division.

Suggested Citation

  • Varshni Rajagopal & Jeanette Seiler & Isha Nasa & Simona Cantarella & Jana Theiss & Franziska Herget & Bianca Kaifer & Melina Klostermann & Rainer Will & Martin Schneider & Dominic Helm & Julian König, 2025. "An atlas of RNA-dependent proteins in cell division reveals the riboregulation of mitotic protein-protein interactions," Nature Communications, Nature, vol. 16(1), pages 1-24, December.
    • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-57671-3
    DOI: 10.1038/s41467-025-57671-3
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    References listed on IDEAS

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    1. Thomas Hollin & Steven Abel & Charles Banks & Borislav Hristov & Jacques Prudhomme & Kianna Hales & Laurence Florens & William Stafford Noble & Karine G. Le Roch, 2024. "Proteome-Wide Identification of RNA-dependent proteins and an emerging role for RNAs in Plasmodium falciparum protein complexes," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    2. Joel I. Perez-Perri & Birgit Rogell & Thomas Schwarzl & Frank Stein & Yang Zhou & Mandy Rettel & Annika Brosig & Matthias W. Hentze, 2018. "Discovery of RNA-binding proteins and characterization of their dynamic responses by enhanced RNA interactome capture," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    3. Benedikt M. Beckmann & Rastislav Horos & Bernd Fischer & Alfredo Castello & Katrin Eichelbaum & Anne-Marie Alleaume & Thomas Schwarzl & Tomaž Curk & Sophia Foehr & Wolfgang Huber & Jeroen Krijgsveld &, 2015. "The RNA-binding proteomes from yeast to man harbour conserved enigmRBPs," Nature Communications, Nature, vol. 6(1), pages 1-9, December.
    4. Björn Schwanhäusser & Dorothea Busse & Na Li & Gunnar Dittmar & Johannes Schuchhardt & Jana Wolf & Wei Chen & Matthias Selbach, 2011. "Global quantification of mammalian gene expression control," Nature, Nature, vol. 473(7347), pages 337-342, May.
    5. Thomas Conrad & Anne-Susann Albrecht & Veronica Rodrigues de Melo Costa & Sascha Sauer & David Meierhofer & Ulf Andersson Ørom, 2016. "Serial interactome capture of the human cell nucleus," Nature Communications, Nature, vol. 7(1), pages 1-11, September.
    6. Lovorka Stojic & Aaron T. L. Lun & Patrice Mascalchi & Christina Ernst & Aisling M. Redmond & Jasmin Mangei & Alexis R. Barr & Vicky Bousgouni & Chris Bakal & John C. Marioni & Duncan T. Odom & Fanni , 2020. "A high-content RNAi screen reveals multiple roles for long noncoding RNAs in cell division," Nature Communications, Nature, vol. 11(1), pages 1-21, December.
    7. Matthew R. King & Sabine Petry, 2020. "Phase separation of TPX2 enhances and spatially coordinates microtubule nucleation," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
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