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PreprintCited by 15Microtubule and mitosis dynamicsRNA Research and SplicingBiotin and Related Studies

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

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Rajagopal, Varshni, Seiler, Jeanette, Nasa, Isha, Cantarella, Simona, Theiss, Jana, Herget, Franziska, Kaifer, Bianca, Schneider, Martin, Helm, Dominic, König, Julian, Zarnack, Kathi, Diederichs, Sven, Kettenbach, Arminja N., Caudron-Herger, Maïwen·2024·Nature Communications
DOI 10.1101/2024.09.25.614981PMC PMC11890761

Preprint — published as 10.1038/s41467-025-57671-3

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Abstract

Ribonucleoprotein complexes are dynamic assemblies of RNA with RNA-binding proteins (RBPs), which can modulate the fate of the RNA molecules from transcription to degradation. Vice versa, RNA can regulate the interactions and functions of the associated proteins. Dysregulation of RBPs is linked to diseases such as cancer and neurological disorders. RNA and RBPs are present in mitotic structures like the centrosomes and spindle microtubules, but their influence on mitotic spindle integrity remains unknown. Thus, we applied the R-DeeP strategy for the proteome-wide identification of RNA-dependent proteins and complexes to cells synchronized in mitosis versus interphase. The resulting atlas of RNA-dependent proteins in cell division can be accessed through the R-DeeP 3.0 database (R-DeeP3.dkfz.de). It revealed key mitotic factors as RNA-dependent such as AURKA, KIFC1 and TPX2 that were linked to RNA despite their lack of canonical RNA-binding domains. KIFC1 was identified as a new interaction partner and phosphorylation substrate of AURKA at S 349 and T 359 . In addition, KIFC1 interacted with both, AURKA and TPX2, in an RNA-dependent manner. Our data suggest a riboregulation of mitotic protein-protein interactions during spindle assembly, offering new perspectives on the control of cell division processes by RNA-protein complexes. Highlights: Differential R-DeeP screens in mitosis and interphase are provided as a resource in a user-friendly database at R-DeeP3.dkfz.de An atlas of RNA-dependent proteins in cell division identifies a substantial number of unconventional RNA-binding proteins among mitotic factors Investigation of protein-protein interactions reveals KIFC1 as a new AURKA and TPX2 interaction partner during spindle assembly KIFC1, AURKA and TPX2 interact with each other in an RNA-dependent manner and directly bind to RNA AURKA phosphorylates KIFC1 at residues S 349 and T 359

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Metadata

Authors
Rajagopal, V., Seiler, J., Nasa, I., Cantarella, S., Theiss, J., Herget, F., Kaifer, B., Schneider, M., Helm, D., König, J., Zarnack, K., Diederichs, S., Kettenbach, A. N., & Caudron-Herger, M.
Affiliations
  • German Cancer Research Center (DE)
  • Dartmouth College (US)
  • University of Würzburg (DE)
  • Goethe University Frankfurt (DE)
  • University of Freiburg (DE)
Corresponding author
  • Diederichs, Sven
  • Kettenbach, Arminja N.
ORCID
Venue
Nature Communications
Publisher
openRxiv
Published
2024-09-26
Volume
16
Issue
1
Pages
2325-2325
ISSN
2041-1723 (ISSN-L)
DOI
10.1101/2024.09.25.614981
PMC
PMC11890761
OpenAlex
W4408247125
Cited by
15
References
1
Citations by year
2026: 8 · 2025: 7
FWCI
7.45
Type
journal article
Language
en
Open access
Licence
Locations
  • Nature Communications (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • PubMed Central (submittedVersion, cc-by-nc-nd)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • FreiDok plus (Universitätsbibliothek Freiburg) (submittedVersion)
Funders
  • U.S. Department of Health and Human Services (R35 GM119455)
  • Baden-Württemberg Stiftung (BWST-ISF2019-027)
  • Center for Strategic Scientific Initiatives, National Cancer Institute (P30CA023108 DCC Core grant)
  • Deutsches Krebsforschungszentrum
  • Deutsche Forschungsgemeinschaft (DFG ZA 881/6-1 (project 541627224), DFG ZA 881/6-1)
  • Israel Science Foundation
  • Deutsche Krebshilfe (70113919)
  • National Institutes of Health
  • National Cancer Institute (P30CA023108)
  • National Institute of General Medical Sciences (R35GM119455)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Biotin and Related Studies
Keywords
RNA-binding proteins, ribonucleoprotein complexes, mitosis, cell division, protein-protein interaction, AURKA, KIFC1, TPX2, kinase regulation, protein stabilization

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