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PreprintCited by 1Microtubule and mitosis dynamicsGenomics and Chromatin DynamicsBiotin and Related Studies

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KIF2C-induced nuclear condensation concentrates PLK1 and phosphorylated BRCA2 at the kinetochore microtubules in mitosis

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Skobelkina, Anastasiia, Julien, Manon, Jeannin, Sylvain, Miron, Simona, Egger, Tom, Chaaban, Rady, Bouvignies, Guillaume, Ghouil, Rania, Friel, Claire, Busso, Didier, Theillet, François-Xavier, Le Bars, Romain, Carreira, Aura, Constantinou, Angelos, Basbous, Jihane, Zinn-Justin, Sophie·2024·Nucleic Acids Research
DOI 10.1101/2024.04.13.589357PMC PMC12153341

Preprint — published as 10.1093/nar/gkaf476 · Paper page

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Abstract

SUMMARY: During mitosis, the human microtubule depolymerase KIF2C increases the turnover of kinetochore-microtubule attachments. This facilitates the correction of attachment errors. Moreover, BRCA2 phosphorylated at Thr207 by PLK1 (BRCA2-pT207) assembles a complex including PLK1, PP2A and BUBR1 that contributes to the stability of the kinetochore-microtubule attachments. PLK1, together with Aurora B, critically regulate the accurate segregation of chromosomes. Here we demonstrate that KIF2C contains an N-terminal domain that binds directly to several phosphorylated peptides, including BRCA2-pT207. Using an optogenetic platform, we reveal that KIF2C assembles into membrane-less compartments or biomolecular condensates that are located next to microtubules. We provide evidence that condensate assembly depends on the presence of the newly defined N-terminal phospho-binding domain of KIF2C and on the kinase activities of Aurora B and PLK1. Moreover, KIF2C condensates concentrate active PLK1 and colocalize with BRCA2-pT207. We propose that, because of its phospho-dependent binding and oligomerization capacities, KIF2C forms biomolecular condensates that partition PLK1 and locally amplify its kinase activity during mitosis. Graphical Abstract:

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Metadata

Authors
Skobelkina, A., Julien, M., Jeannin, S., Miron, S., Egger, T., Chaaban, R., Bouvignies, G., Ghouil, R., Friel, C., Busso, D., Theillet, F.-X., Le Bars, R., Carreira, A., Constantinou, A., Basbous, J., & Zinn-Justin, S.
Affiliations
  • Centre National de la Recherche Scientifique (FR)
  • University of Nottingham (GB)
  • Inserm (FR)
Corresponding author
Basbous, Jihane
ORCID
Venue
Nucleic Acids Research
Publisher
openRxiv
Published
2024-04-14
Volume
53
Issue
11
Pages
gkaf476
ISSN
0305-1048 (ISSN-L)
DOI
10.1101/2024.04.13.589357
PMC
PMC12153341
OpenAlex
W4411209503
Cited by
1
References
1
Citations by year
2026: 1
FWCI
0.50
Type
journal article
Language
en
Open access
Licence
cc-by-nc
Locations
  • Nucleic Acids Research (publishedVersion, cc-by-nc)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by-nc)
  • PubMed (publishedVersion)
  • DIGITAL.CSIC (Spanish National Research Council (CSIC)) (publishedVersion, other-oa)
  • Repository@Nottingham (University of Nottingham) (publishedVersion, cc-by-nc)
  • Repository@Nottingham (University of Nottingham) (submittedVersion, cc-by-nc)
  • HAL (submittedVersion)
  • HAL (submittedVersion, cc-by-nc)
Funders
  • Biogen
  • California Earthquake Authority
  • Agence Nationale de la Recherche (ANR-10-INSB-05-01., ANR-23-CE12-0032, ANR-11-EQPX-0029, ANR-21-CE12-0023, 10-INSB-05-01, ANR- 10-INSB-05, ANR???11???IDEX???0003???02, ANR-11-IDEX-0003, AAPG2023, ANR-17-EURE-0007, ANR‐10_INBS‐04, ANR-11-IDEX, AAPG2021, ANR-10, ANR-24-INBS-0005, ANR-10-INBS-0005)
  • Institut National de la Santé et de la Recherche Médicale (PCSI 2022)
  • Fondation pour la Recherche Médicale (N°FDT202304016927)
  • Centre National de la Recherche Scientifique (FR 2054, 11-IDEX-0003)
  • Institut National Du Cancer (PLBIO2021, PCSI 2022)
  • French Infrastructure for Integrated Structural Biology (ANR-10- INSB-05, ANR-10-INSB-0501, INSB-05)
  • College of Natural Resources and Sciences, Humboldt State University
  • National Cancer Institute
  • Division of Arctic Sciences (N°248989)
  • Vermont Agency of Natural Resources (ANR-21-CEA13-0030)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Biotin and Related Studies
Keywords
KIF2C, PLK1, kinetochore-microtubule attachment, mitosis, biomolecular condensates, condensate, Aurora B kinase, microtubule depolymerase, chromosome alignment, chromosome stability, optogenetics
MeSH terms
Polo-Like Kinase 1, HeLa Cells, Humans, Microtubules, Mitosis, Phosphorylation, Protein Binding, Proto-Oncogene Proteins, Kinesins, Protein Serine-Threonine Kinases, Kinetochores, Cell Cycle Proteins, BRCA2 Protein, Aurora Kinase B

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