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FIGNL1 AAA+ ATPase remodels RAD51 and DMC1 filaments in pre-meiotic DNA replication and meiotic recombination

Author

Listed:
  • Masaru Ito

    (Osaka University, Suita)

  • Asako Furukohri

    (Osaka University, Suita)

  • Kenichiro Matsuzaki

    (Osaka University, Suita
    Kindai University, Nara)

  • Yurika Fujita

    (Osaka University, Suita)

  • Atsushi Toyoda

    (National Institute of Genetics, Mishima)

  • Akira Shinohara

    (Osaka University, Suita)

Abstract

The formation of RAD51/DMC1 filaments on single-stranded (ss)DNAs essential for homology search and strand exchange in DNA double-strand break (DSB) repair is tightly regulated. FIGNL1 AAA+++ ATPase controls RAD51-mediated recombination in human cells. However, its role in gametogenesis remains unsolved. Here, we characterized a germ line-specific conditional knockout (cKO) mouse of FIGNL1. Fignl1 cKO male mice showed defective chromosome synapsis and impaired meiotic DSB repair with the accumulation of RAD51/DMC1 on meiotic chromosomes, supporting a positive role of FIGNL1 in homologous recombination at a post-assembly stage of RAD51/DMC1 filaments. Fignl1 cKO spermatocytes also accumulate RAD51/DMC1 on chromosomes in pre-meiotic S-phase. These RAD51/DMC1 assemblies are independent of meiotic DSB formation. We also showed that purified FIGNL1 dismantles RAD51 filament on double-stranded (ds)DNA as well as ssDNA. These results suggest an additional role of FIGNL1 in limiting the non-productive assembly of RAD51/DMC1 on native dsDNAs during pre-meiotic S-phase and meiotic prophase I.

Suggested Citation

  • Masaru Ito & Asako Furukohri & Kenichiro Matsuzaki & Yurika Fujita & Atsushi Toyoda & Akira Shinohara, 2023. "FIGNL1 AAA+ ATPase remodels RAD51 and DMC1 filaments in pre-meiotic DNA replication and meiotic recombination," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42576-w
    DOI: 10.1038/s41467-023-42576-w
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    1. Mengcheng Luo & Fang Yang & N. Adrian Leu & Jessica Landaiche & Mary Ann Handel & Ricardo Benavente & Sophie La Salle & P. Jeremy Wang, 2013. "MEIOB exhibits single-stranded DNA-binding and exonuclease activities and is essential for meiotic recombination," Nature Communications, Nature, vol. 4(1), pages 1-12, December.
    2. Fatima Smagulova & Ivan V. Gregoretti & Kevin Brick & Pavel Khil & R. Daniel Camerini-Otero & Galina V. Petukhova, 2011. "Genome-wide analysis reveals novel molecular features of mouse recombination hotspots," Nature, Nature, vol. 472(7343), pages 375-378, April.
    3. Akira Shinohara & Tomoko Ogawa, 1998. "Stimulation by Rad52 of yeast Rad51- mediated recombination," Nature, Nature, vol. 391(6665), pages 404-407, January.
    4. Rohit Prakash & Thomas Sandoval & Florian Morati & Jennifer A. Zagelbaum & Pei-Xin Lim & Travis White & Brett Taylor & Raymond Wang & Emilie C. B. Desclos & Meghan R. Sullivan & Hayley L. Rein & Kara , 2021. "Distinct pathways of homologous recombination controlled by the SWS1–SWSAP1–SPIDR complex," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    5. Carla M. Abreu & Rohit Prakash & Peter J. Romanienko & Ignasi Roig & Scott Keeney & Maria Jasin, 2018. "Shu complex SWS1-SWSAP1 promotes early steps in mouse meiotic recombination," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    6. Weixing Zhao & Justin B. Steinfeld & Fengshan Liang & Xiaoyong Chen & David G. Maranon & Chu Jian Ma & Youngho Kwon & Timsi Rao & Weibin Wang & Chen Sheng & Xuemei Song & Yanhong Deng & Judit Jimenez-, 2017. "BRCA1–BARD1 promotes RAD51-mediated homologous DNA pairing," Nature, Nature, vol. 550(7676), pages 360-365, October.
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