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DNA-dependent macromolecular condensation drives self-assembly of the meiotic DNA break machinery

View ORCID ProfileCorentin Claeys Bouuaert, Stephen Pu, Juncheng Wang, Dinshaw J. Patel, View ORCID ProfileScott Keeney
doi: https://doi.org/10.1101/2020.02.21.960245
Corentin Claeys Bouuaert
1Molecular Biology Program, Memorial Sloan Kettering Cancer Center and Howard Hughes Medical Institute, New York, US
2Louvain Institute of Biomolecular Science and Technology, Université catholique de Louvain, Louvain-La-Neuve, Belgium
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  • ORCID record for Corentin Claeys Bouuaert
  • For correspondence: corentin.claeys@uclouvain.be s-keeney@ski.mskcc.org
Stephen Pu
1Molecular Biology Program, Memorial Sloan Kettering Cancer Center and Howard Hughes Medical Institute, New York, US
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Juncheng Wang
3Structural Biology Program, Memorial Sloan Kettering Cancer Center, New York, US
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Dinshaw J. Patel
3Structural Biology Program, Memorial Sloan Kettering Cancer Center, New York, US
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Scott Keeney
1Molecular Biology Program, Memorial Sloan Kettering Cancer Center and Howard Hughes Medical Institute, New York, US
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  • ORCID record for Scott Keeney
  • For correspondence: corentin.claeys@uclouvain.be s-keeney@ski.mskcc.org
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Abstract

Formation of meiotic DNA double-strand breaks (DSBs) by Spo11 is tightly regulated and tied to chromosome structure, but the higher-order assemblies that execute and control DNA breakage are poorly understood. We address this question through molecular characterization of Saccharomyces cerevisiae RMM proteins (Rec114, Mei4 and Mer2)—essential, conserved components of the DSB machinery. Each subcomplex of Rec114–Mei4 (2:1 heterotrimer) or Mer2 (homotetrameric coiled coil) is monodisperse in solution, but they independently condense with DNA into dynamic, reversible nucleoprotein clusters that share properties with phase-separated systems. Multivalent interactions drive condensation, which correlates with DSB formation in vivo. Condensates fuse into mixed Rec114–Mei4–Mer2 clusters that further recruit Spo11 complexes. Our data show how the DSB machinery self-assembles on chromosome axes to create centers of DSB activity. We propose that multilayered control of Spo11 arises from recruitment of regulatory components and modulation of biophysical properties of the condensates.

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Posted February 24, 2020.
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DNA-dependent macromolecular condensation drives self-assembly of the meiotic DNA break machinery
Corentin Claeys Bouuaert, Stephen Pu, Juncheng Wang, Dinshaw J. Patel, Scott Keeney
bioRxiv 2020.02.21.960245; doi: https://doi.org/10.1101/2020.02.21.960245
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DNA-dependent macromolecular condensation drives self-assembly of the meiotic DNA break machinery
Corentin Claeys Bouuaert, Stephen Pu, Juncheng Wang, Dinshaw J. Patel, Scott Keeney
bioRxiv 2020.02.21.960245; doi: https://doi.org/10.1101/2020.02.21.960245

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