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Nuclear myosin VI maintains replication fork stability

Author

Listed:
  • Jie Shi

    (Institute of Molecular Biology gGmbH (IMB))

  • Kristine Hauschulte

    (Institute of Molecular Biology gGmbH (IMB))

  • Ivan Mikicic

    (Institute of Molecular Biology gGmbH (IMB))

  • Srijana Maharjan

    (Institute of Molecular Biology gGmbH (IMB)
    Mainz Biomed N.V.)

  • Valerie Arz

    (Institute of Molecular Biology gGmbH (IMB))

  • Tina Strauch

    (Institute of Molecular Biology gGmbH (IMB))

  • Jan B. Heidelberger

    (Institute of Molecular Biology gGmbH (IMB)
    Max Planck School Matter to Life)

  • Jonas V. Schaefer

    (Department of Biochemistry)

  • Birgit Dreier

    (Department of Biochemistry)

  • Andreas Plückthun

    (Department of Biochemistry)

  • Petra Beli

    (Institute of Molecular Biology gGmbH (IMB)
    Johannes Gutenberg University)

  • Helle D. Ulrich

    (Institute of Molecular Biology gGmbH (IMB))

  • Hans-Peter Wollscheid

    (Institute of Molecular Biology gGmbH (IMB))

Abstract

The actin cytoskeleton is of fundamental importance for cellular structure and plasticity. However, abundance and function of filamentous actin in the nucleus are still controversial. Here we show that the actin-based molecular motor myosin VI contributes to the stabilization of stalled or reversed replication forks. In response to DNA replication stress, myosin VI associates with stalled replication intermediates and cooperates with the AAA ATPase Werner helicase interacting protein 1 (WRNIP1) in protecting these structures from DNA2-mediated nucleolytic attack. Using functionalized affinity probes to manipulate myosin VI levels in a compartment-specific manner, we provide evidence for the direct involvement of myosin VI in the nucleus and against a contribution of the abundant cytoplasmic pool during the replication stress response.

Suggested Citation

  • Jie Shi & Kristine Hauschulte & Ivan Mikicic & Srijana Maharjan & Valerie Arz & Tina Strauch & Jan B. Heidelberger & Jonas V. Schaefer & Birgit Dreier & Andreas Plückthun & Petra Beli & Helle D. Ulric, 2023. "Nuclear myosin VI maintains replication fork stability," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39517-y
    DOI: 10.1038/s41467-023-39517-y
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    References listed on IDEAS

    as
    1. Christopher P. Caridi & Carla D’Agostino & Taehyun Ryu & Grzegorz Zapotoczny & Laetitia Delabaere & Xiao Li & Varandt Y. Khodaverdian & Nuno Amaral & Emily Lin & Alesandra R. Rau & Irene Chiolo, 2018. "Nuclear F-actin and myosins drive relocalization of heterochromatic breaks," Nature, Nature, vol. 559(7712), pages 54-60, July.
    2. Yukti Hari-Gupta & Natalia Fili & Ália dos Santos & Alexander W. Cook & Rosemarie E. Gough & Hannah C. W. Reed & Lin Wang & Jesse Aaron & Tomas Venit & Eric Wait & Andreas Grosse-Berkenbusch & J. Chri, 2022. "Myosin VI regulates the spatial organisation of mammalian transcription initiation," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    3. Benjamin R. Schrank & Tomas Aparicio & Yinyin Li & Wakam Chang & Brian T. Chait & Gregg G. Gundersen & Max E. Gottesman & Jean Gautier, 2018. "Nuclear ARP2/3 drives DNA break clustering for homology-directed repair," Nature, Nature, vol. 559(7712), pages 61-66, July.
    4. Natalia Fili & Yukti Hari-Gupta & Ália dos Santos & Alexander Cook & Simon Poland & Simon M. Ameer-Beg & Maddy Parsons & Christopher P. Toseland, 2017. "NDP52 activates nuclear myosin VI to enhance RNA polymerase II transcription," Nature Communications, Nature, vol. 8(1), pages 1-15, December.
    5. Amber L. Wells & Abel W. Lin & Li-Qiong Chen & Daniel Safer & Shane M. Cain & Tama Hasson & Bridget O. Carragher & Ronald A. Milligan & H. Lee Sweeney, 1999. "Myosin VI is an actin-based motor that moves backwards," Nature, Nature, vol. 401(6752), pages 505-508, September.
    6. Seong-Su Han & Kuo-Kuang Wen & María L. García-Rubio & Marc S. Wold & Andrés Aguilera & Wojciech Niedzwiedz & Yatin M. Vyas, 2022. "WASp modulates RPA function on single-stranded DNA in response to replication stress and DNA damage," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
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    1. Maria Dilia Palumbieri & Chiara Merigliano & Daniel González-Acosta & Danina Kuster & Jana Krietsch & Henriette Stoy & Thomas Känel & Svenja Ulferts & Bettina Welter & Joël Frey & Cyril Doerdelmann & , 2023. "Nuclear actin polymerization rapidly mediates replication fork remodeling upon stress by limiting PrimPol activity," Nature Communications, Nature, vol. 14(1), pages 1-15, December.

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