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Mitotic chromosome binding predicts transcription factor properties in interphase

Author

Listed:
  • Mahé Raccaud

    (Ecole Polytechnique Fédérale de Lausanne (EPFL))

  • Elias T. Friman

    (Ecole Polytechnique Fédérale de Lausanne (EPFL))

  • Andrea B. Alber

    (Ecole Polytechnique Fédérale de Lausanne (EPFL))

  • Harsha Agarwal

    (Ulm University)

  • Cédric Deluz

    (Ecole Polytechnique Fédérale de Lausanne (EPFL))

  • Timo Kuhn

    (Ulm University)

  • J. Christof M. Gebhardt

    (Ulm University)

  • David M. Suter

    (Ecole Polytechnique Fédérale de Lausanne (EPFL))

Abstract

Mammalian transcription factors (TFs) differ broadly in their nuclear mobility and sequence-specific/non-specific DNA binding. How these properties affect their ability to occupy specific genomic sites and modify the epigenetic landscape is unclear. The association of TFs with mitotic chromosomes observed by fluorescence microscopy is largely mediated by non-specific DNA interactions and differs broadly between TFs. Here we combine quantitative measurements of mitotic chromosome binding (MCB) of 501 TFs, TF mobility measurements by fluorescence recovery after photobleaching, single molecule imaging of DNA binding, and mapping of TF binding and chromatin accessibility. TFs associating to mitotic chromosomes are enriched in DNA-rich compartments in interphase and display slower mobility in interphase and mitosis. Remarkably, MCB correlates with relative TF on-rates and genome-wide specific site occupancy, but not with TF residence times. This suggests that non-specific DNA binding properties of TFs regulate their search efficiency and occupancy of specific genomic sites.

Suggested Citation

  • Mahé Raccaud & Elias T. Friman & Andrea B. Alber & Harsha Agarwal & Cédric Deluz & Timo Kuhn & J. Christof M. Gebhardt & David M. Suter, 2019. "Mitotic chromosome binding predicts transcription factor properties in interphase," Nature Communications, Nature, vol. 10(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-019-08417-5
    DOI: 10.1038/s41467-019-08417-5
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    Cited by:

    1. Rebecca J. Harris & Maninder Heer & Mark D. Levasseur & Tyrell N. Cartwright & Bethany Weston & Jennifer L. Mitchell & Jonathan M. Coxhead & Luke Gaughan & Lisa Prendergast & Daniel Rico & Jonathan M., 2023. "Release of Histone H3K4-reading transcription factors from chromosomes in mitosis is independent of adjacent H3 phosphorylation," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    2. Andrea Riba & Attila Oravecz & Matej Durik & Sara Jiménez & Violaine Alunni & Marie Cerciat & Matthieu Jung & Céline Keime & William M. Keyes & Nacho Molina, 2022. "Cell cycle gene regulation dynamics revealed by RNA velocity and deep-learning," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    3. Kian Hong Kock & Patrick K. Kimes & Stephen S. Gisselbrecht & Sachi Inukai & Sabrina K. Phanor & James T. Anderson & Gayatri Ramakrishnan & Colin H. Lipper & Dongyuan Song & Jesse V. Kurland & Julia M, 2024. "DNA binding analysis of rare variants in homeodomains reveals homeodomain specificity-determining residues," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    4. Rita Silvério-Alves & Ilia Kurochkin & Anna Rydström & Camila Vazquez Echegaray & Jakob Haider & Matthew Nicholls & Christina Rode & Louise Thelaus & Aida Yifter Lindgren & Alexandra Gabriela Ferreira, 2023. "GATA2 mitotic bookmarking is required for definitive haematopoiesis," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    5. Maëlle Bellec & Jérémy Dufourt & George Hunt & Hélène Lenden-Hasse & Antonio Trullo & Amal Zine El Aabidine & Marie Lamarque & Marissa M. Gaskill & Heloïse Faure-Gautron & Mattias Mannervik & Melissa , 2022. "The control of transcriptional memory by stable mitotic bookmarking," Nature Communications, Nature, vol. 13(1), pages 1-14, December.

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