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Release of Histone H3K4-reading transcription factors from chromosomes in mitosis is independent of adjacent H3 phosphorylation

Author

Listed:
  • Rebecca J. Harris

    (Newcastle University)

  • Maninder Heer

    (Newcastle University)

  • Mark D. Levasseur

    (Newcastle University)

  • Tyrell N. Cartwright

    (Newcastle University)

  • Bethany Weston

    (Newcastle University)

  • Jennifer L. Mitchell

    (Newcastle University)

  • Jonathan M. Coxhead

    (Newcastle University)

  • Luke Gaughan

    (Newcastle University
    Newcastle University Centre for Cancer, Faculty of Medical Sciences)

  • Lisa Prendergast

    (Newcastle University)

  • Daniel Rico

    (Newcastle University
    Newcastle University Centre for Cancer, Faculty of Medical Sciences
    CSIC-Universidad Sevilla-Universidad Pablo de Olavide-Junta de Andalucía)

  • Jonathan M. G. Higgins

    (Newcastle University
    Newcastle University Centre for Cancer, Faculty of Medical Sciences)

Abstract

Histone modifications influence the recruitment of reader proteins to chromosomes to regulate events including transcription and cell division. The idea of a histone code, where combinations of modifications specify unique downstream functions, is widely accepted and can be demonstrated in vitro. For example, on synthetic peptides, phosphorylation of Histone H3 at threonine-3 (H3T3ph) prevents the binding of reader proteins that recognize trimethylation of the adjacent lysine-4 (H3K4me3), including the TAF3 component of TFIID. To study these combinatorial effects in cells, we analyzed the genome-wide distribution of H3T3ph and H3K4me2/3 during mitosis. We find that H3T3ph anti-correlates with adjacent H3K4me2/3 in cells, and that the PHD domain of TAF3 can bind H3K4me2/3 in isolated mitotic chromatin despite the presence of H3T3ph. Unlike in vitro, H3K4 readers are still displaced from chromosomes in mitosis in Haspin-depleted cells lacking H3T3ph. H3T3ph is therefore unlikely to be responsible for transcriptional downregulation during cell division.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43115-3
    DOI: 10.1038/s41467-023-43115-3
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    References listed on IDEAS

    as
    1. Hua Wang & Zheng Fan & Pavel V. Shliaha & Matthew Miele & Ronald C. Hendrickson & Xuejun Jiang & Kristian Helin, 2023. "Publisher Correction: H3K4me3 regulates RNA polymerase II promoter-proximal pause-release," Nature, Nature, vol. 616(7956), pages 7-7, April.
    2. Hua Wang & Zheng Fan & Pavel V. Shliaha & Matthew Miele & Ronald C. Hendrickson & Xuejun Jiang & Kristian Helin, 2023. "H3K4me3 regulates RNA polymerase II promoter-proximal pause-release," Nature, Nature, vol. 615(7951), pages 339-348, March.
    3. 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.
    4. Takashi Nagano & Yaniv Lubling & Csilla Várnai & Carmel Dudley & Wing Leung & Yael Baran & Netta Mendelson Cohen & Steven Wingett & Peter Fraser & Amos Tanay, 2017. "Cell-cycle dynamics of chromosomal organization at single-cell resolution," Nature, Nature, vol. 547(7661), pages 61-67, July.
    5. Paul Adrian Ginno & Lukas Burger & Jan Seebacher & Vytautas Iesmantavicius & Dirk Schübeler, 2018. "Cell cycle-resolved chromatin proteomics reveals the extent of mitotic preservation of the genomic regulatory landscape," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    6. Toru Hirota & Jesse J. Lipp & Ban-Hock Toh & Jan-Michael Peters, 2005. "Histone H3 serine 10 phosphorylation by Aurora B causes HP1 dissociation from heterochromatin," Nature, Nature, vol. 438(7071), pages 1176-1180, December.
    7. Dounia Djeghloul & Bhavik Patel & Holger Kramer & Andrew Dimond & Chad Whilding & Karen Brown & Anne-Céline Kohler & Amelie Feytout & Nicolas Veland & James Elliott & Tanmay A. M. Bharat & Abul K. Tar, 2020. "Identifying proteins bound to native mitotic ESC chromosomes reveals chromatin repressors are important for compaction," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    8. Wolfgang Fischle & Boo Shan Tseng & Holger L. Dormann & Beatrix M. Ueberheide & Benjamin A. Garcia & Jeffrey Shabanowitz & Donald F. Hunt & Hironori Funabiki & C. David Allis, 2005. "Regulation of HP1–chromatin binding by histone H3 methylation and phosphorylation," Nature, Nature, vol. 438(7071), pages 1116-1122, December.
    9. Takashi Sutani & Toyonori Sakata & Ryuichiro Nakato & Koji Masuda & Mai Ishibashi & Daisuke Yamashita & Yutaka Suzuki & Tatsuya Hirano & Masashige Bando & Katsuhiko Shirahige, 2015. "Condensin targets and reduces unwound DNA structures associated with transcription in mitotic chromosome condensation," Nature Communications, Nature, vol. 6(1), pages 1-13, November.
    10. Emil F. Michelotti & Suzanne Sanford & David Levens, 1997. "Marking of active genes on mitotic chromosomes," Nature, Nature, vol. 388(6645), pages 895-899, August.
    11. Haoyue Zhang & Daniel J. Emerson & Thomas G. Gilgenast & Katelyn R. Titus & Yemin Lan & Peng Huang & Di Zhang & Hongxin Wang & Cheryl A. Keller & Belinda Giardine & Ross C. Hardison & Jennifer E. Phil, 2019. "Chromatin structure dynamics during the mitosis-to-G1 phase transition," Nature, Nature, vol. 576(7785), pages 158-162, December.
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