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Seeding the meiotic DNA break machinery and initiating recombination on chromosome axes

Author

Listed:
  • Ihsan Dereli

    (Faculty of Medicine at the TU Dresden)

  • Vladyslav Telychko

    (Faculty of Medicine at the TU Dresden)

  • Frantzeskos Papanikos

    (Faculty of Medicine at the TU Dresden)

  • Kavya Raveendran

    (Faculty of Medicine at the TU Dresden)

  • Jiaqi Xu

    (Memorial Sloan Kettering Cancer Center
    Weill Cornell Graduate School of Medical Sciences)

  • Michiel Boekhout

    (Memorial Sloan Kettering Cancer Center)

  • Marcello Stanzione

    (Faculty of Medicine at the TU Dresden)

  • Benjamin Neuditschko

    (IMC University of Applied Sciences)

  • Naga Sailaja Imjeti

    (Faculty of Medicine at the TU Dresden)

  • Elizaveta Selezneva

    (Friedrich Miescher Laboratory of the Max Planck Society)

  • Hasibe Tuncay

    (University of Hamburg)

  • Sevgican Demir

    (Faculty of Medicine at the TU Dresden)

  • Teresa Giannattasio

    (Section of Anatomy)

  • Marc Gentzel

    (Technische Universität Dresden)

  • Anastasiia Bondarieva

    (Faculty of Medicine at the TU Dresden)

  • Michelle Stevense

    (Faculty of Medicine at the TU Dresden)

  • Marco Barchi

    (Section of Anatomy
    Saint Camillus International University of Health Sciences)

  • Arp Schnittger

    (University of Hamburg)

  • John R. Weir

    (Friedrich Miescher Laboratory of the Max Planck Society)

  • Franz Herzog

    (IMC University of Applied Sciences)

  • Scott Keeney

    (Memorial Sloan Kettering Cancer Center
    Weill Cornell Graduate School of Medical Sciences
    Memorial Sloan Kettering Cancer Center)

  • Attila Tóth

    (Faculty of Medicine at the TU Dresden)

Abstract

Programmed DNA double-strand break (DSB) formation is a crucial feature of meiosis in most organisms. DSBs initiate recombination-mediated linking of homologous chromosomes, which enables correct chromosome segregation in meiosis. DSBs are generated on chromosome axes by heterooligomeric focal clusters of DSB-factors. Whereas DNA-driven protein condensation is thought to assemble the DSB-machinery, its targeting to chromosome axes is poorly understood. We uncover in mice that efficient biogenesis of DSB-machinery clusters requires seeding by axial IHO1 platforms. Both IHO1 phosphorylation and formation of axial IHO1 platforms are diminished by chemical inhibition of DBF4-dependent kinase (DDK), suggesting that DDK contributes to the control of the axial DSB-machinery. Furthermore, we show that axial IHO1 platforms are based on an interaction between IHO1 and the chromosomal axis component HORMAD1. IHO1-HORMAD1-mediated seeding of the DSB-machinery on axes ensures sufficiency of DSBs for efficient pairing of homologous chromosomes. Without IHO1-HORMAD1 interaction, residual DSBs depend on ANKRD31, which enhances both the seeding and the growth of DSB-machinery clusters. Thus, recombination initiation is ensured by complementary pathways that differentially support seeding and growth of DSB-machinery clusters, thereby synergistically enabling DSB-machinery condensation on chromosomal axes.

Suggested Citation

  • Ihsan Dereli & Vladyslav Telychko & Frantzeskos Papanikos & Kavya Raveendran & Jiaqi Xu & Michiel Boekhout & Marcello Stanzione & Benjamin Neuditschko & Naga Sailaja Imjeti & Elizaveta Selezneva & Has, 2024. "Seeding the meiotic DNA break machinery and initiating recombination on chromosome axes," Nature Communications, Nature, vol. 15(1), pages 1-23, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47020-1
    DOI: 10.1038/s41467-024-47020-1
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    References listed on IDEAS

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