IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-42576-w.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-42576-w
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-42576-w?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    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. Akira Shinohara & Tomoko Ogawa, 1998. "Stimulation by Rad52 of yeast Rad51- mediated recombination," Nature, Nature, vol. 391(6665), pages 404-407, January.
    3. 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.
    4. 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.
    5. 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.
    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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Wu Zuo & Guangming Chen & Zhimei Gao & Shuai Li & Yanyan Chen & Chenhui Huang & Juan Chen & Zhengjun Chen & Ming Lei & Qian Bian, 2021. "Stage-resolved Hi-C analyses reveal meiotic chromosome organizational features influencing homolog alignment," Nature Communications, Nature, vol. 12(1), pages 1-20, December.
    2. George E. Ronson & Katarzyna Starowicz & Elizabeth J. Anthony & Ann Liza Piberger & Lucy C. Clarke & Alexander J. Garvin & Andrew D. Beggs & Celina M. Whalley & Matthew J. Edmonds & James F. J. Beesle, 2023. "Mechanisms of synthetic lethality between BRCA1/2 and 53BP1 deficiencies and DNA polymerase theta targeting," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    3. Scisung Chung & Mi-Sun Kang & Dauren S. Alimbetov & Gil-Im Mun & Na-Oh Yunn & Yunjin Kim & Byung-Gyu Kim & Minwoo Wie & Eun A. Lee & Jae Sun Ra & Jung-Min Oh & Donghyun Lee & Keondo Lee & Jihan Kim & , 2022. "Regulation of BRCA1 stability through the tandem UBX domains of isoleucyl-tRNA synthetase 1," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    4. Maja Szymanska-Lejman & Wojciech Dziegielewski & Julia Dluzewska & Nadia Kbiri & Anna Bieluszewska & R. Scott Poethig & Piotr A. Ziolkowski, 2023. "The effect of DNA polymorphisms and natural variation on crossover hotspot activity in Arabidopsis hybrids," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    5. Shengli Zhao & Zehui Dong & Yuna Zhao, 2022. "Order-of-Addition Orthogonal Arrays with High Strength," Mathematics, MDPI, vol. 10(7), pages 1-17, April.
    6. Guangxue Liu & Jimin Li & Boxue He & Jiaqi Yan & Jingyu Zhao & Xuejie Wang & Xiaocong Zhao & Jingyan Xu & Yeyao Wu & Simin Zhang & Xiaoli Gan & Chun Zhou & Xiangpan Li & Xinghua Zhang & Xuefeng Chen, 2023. "Bre1/RNF20 promotes Rad51-mediated strand exchange and antagonizes the Srs2/FBH1 helicases," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    7. Jessica D. Tischler & Hiroshi Tsuchida & Rosevalentine Bosire & Tommy T. Oda & Ana Park & Richard O. Adeyemi, 2024. "FLIP(C1orf112)-FIGNL1 complex regulates RAD51 chromatin association to promote viability after replication stress," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    8. Xiao, Qian & Xu, Hongquan, 2021. "A mapping-based universal Kriging model for order-of-addition experiments in drug combination studies," Computational Statistics & Data Analysis, Elsevier, vol. 157(C).
    9. Qian Zhu & Jinzhou Huang & Hongyang Huang & Huan Li & Peiqiang Yi & Jake A. Kloeber & Jian Yuan & Yuping Chen & Min Deng & Kuntian Luo & Ming Gao & Guijie Guo & Xinyi Tu & Ping Yin & Yong Zhang & Jun , 2021. "RNF19A-mediated ubiquitination of BARD1 prevents BRCA1/BARD1-dependent homologous recombination," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    10. Mengwen Hu & Yu-Han Yeh & Yasuhisa Munakata & Hironori Abe & Akihiko Sakashita & So Maezawa & Miguel Vidal & Haruhiko Koseki & Neil Hunter & Richard M. Schultz & Satoshi H. Namekawa, 2022. "PRC1-mediated epigenetic programming is required to generate the ovarian reserve," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    11. Zhen Wang & Claudia M. Castillo-González & Changjiang Zhao & Chun-Yip Tong & Changhao Li & Songxiao Zhong & Zhiyang Liu & Kaili Xie & Jiaying Zhu & Zhongshou Wu & Xu Peng & Yannick Jacob & Scott D. Mi, 2023. "H3.1K27me1 loss confers Arabidopsis resistance to Geminivirus by sequestering DNA repair proteins onto host genome," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    12. Chen, Jianbin & Mukerjee, Rahul & Lin, Dennis K.J., 2020. "Construction of optimal fractional Order-of-Addition designs via block designs," Statistics & Probability Letters, Elsevier, vol. 161(C).

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42576-w. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.