IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-34612-y.html
   My bibliography  Save this article

Regulation of BRCA1 stability through the tandem UBX domains of isoleucyl-tRNA synthetase 1

Author

Listed:
  • Scisung Chung

    (Pohang University of Science and Technology)

  • Mi-Sun Kang

    (Institute for Basic Science (IBS))

  • Dauren S. Alimbetov

    (University of Texas Health San Antonio)

  • Gil-Im Mun

    (Ewha Womans University)

  • Na-Oh Yunn

    (Pohang University of Science and Technology)

  • Yunjin Kim

    (Pohang University of Science and Technology)

  • Byung-Gyu Kim

    (Institute for Basic Science (IBS))

  • Minwoo Wie

    (Institute for Basic Science (IBS))

  • Eun A. Lee

    (Institute for Basic Science (IBS))

  • Jae Sun Ra

    (Institute for Basic Science (IBS))

  • Jung-Min Oh

    (Pusan National University)

  • Donghyun Lee

    (Pohang University of Science and Technology)

  • Keondo Lee

    (Pohang University of Science and Technology)

  • Jihan Kim

    (Pohang University of Science and Technology)

  • Seung Hyun Han

    (Pohang University of Science and Technology)

  • Kyong-Tai Kim

    (Pohang University of Science and Technology)

  • Wan Kyun Chung

    (Pohang University of Science and Technology)

  • Ki Hyun Nam

    (Korea University
    Korea University)

  • Jaehyun Park

    (Pohang University of Science and Technology)

  • ByungHoon Lee

    (Daegu Gyeongbuk Institute of Science and Technology (DGIST))

  • Sunghoon Kim

    (Yonsei University)

  • Weixing Zhao

    (University of Texas Health San Antonio)

  • Sung Ho Ryu

    (Pohang University of Science and Technology)

  • Yun-Sil Lee

    (Ewha Womans University)

  • Kyungjae Myung

    (Institute for Basic Science (IBS)
    Ulsan National Institute of Science and Technology)

  • Yunje Cho

    (Pohang University of Science and Technology)

Abstract

Aminoacyl-tRNA synthetases (ARSs) have evolved to acquire various additional domains. These domains allow ARSs to communicate with other cellular proteins in order to promote non-translational functions. Vertebrate cytoplasmic isoleucyl-tRNA synthetases (IARS1s) have an uncharacterized unique domain, UNE-I. Here, we present the crystal structure of the chicken IARS1 UNE-I complexed with glutamyl-tRNA synthetase 1 (EARS1). UNE-I consists of tandem ubiquitin regulatory X (UBX) domains that interact with a distinct hairpin loop on EARS1 and protect its neighboring proteins in the multi-synthetase complex from degradation. Phosphomimetic mutation of the two serine residues in the hairpin loop releases IARS1 from the complex. IARS1 interacts with BRCA1 in the nucleus, regulates its stability by inhibiting ubiquitylation via the UBX domains, and controls DNA repair function.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34612-y
    DOI: 10.1038/s41467-022-34612-y
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-34612-y
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-34612-y?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. Abul Arif & Fulvia Terenzi & Alka A. Potdar & Jie Jia & Jessica Sacks & Arnab China & Dalia Halawani & Kommireddy Vasu & Xiaoxia Li & J. Mark Brown & Jie Chen & Sara C. Kozma & George Thomas & Paul L., 2017. "EPRS is a critical mTORC1–S6K1 effector that influences adiposity in mice," Nature, Nature, vol. 542(7641), pages 357-361, February.
    2. 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.
    3. Hannah Farmer & Nuala McCabe & Christopher J. Lord & Andrew N. J. Tutt & Damian A. Johnson & Tobias B. Richardson & Manuela Santarosa & Krystyna J. Dillon & Ian Hickson & Charlotte Knights & Niall M. , 2005. "Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy," Nature, Nature, vol. 434(7035), pages 917-921, April.
    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. Zita Gál & Stavroula Boukoura & Kezia Catharina Oxe & Sara Badawi & Blanca Nieto & Lea Milling Korsholm & Sille Blangstrup Geisler & Ekaterina Dulina & Anna Vestergaard Rasmussen & Christina Dahl & We, 2024. "Hyper-recombination in ribosomal DNA is driven by long-range resection-independent RAD51 accumulation," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    2. Neil J. Rzechorzek & Simone Kunzelmann & Andrew G. Purkiss & Mariana Silva Dos Santos & James I. MacRae & Ian A. Taylor & Kasper Fugger & Stephen C. West, 2023. "Mechanism of substrate hydrolysis by the human nucleotide pool sanitiser DNPH1," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    3. Heathcliff Dorado García & Fabian Pusch & Yi Bei & Jennifer Stebut & Glorymar Ibáñez & Kristina Guillan & Koshi Imami & Dennis Gürgen & Jana Rolff & Konstantin Helmsauer & Stephanie Meyer-Liesener & N, 2022. "Therapeutic targeting of ATR in alveolar rhabdomyosarcoma," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    4. Sundarraj Jayakumar & Manthan Patel & Fanny Boulet & Hadicha Aziz & Greg N. Brooke & Hemanth Tummala & Madapura M. Pradeepa, 2024. "PSIP1/LEDGF reduces R-loops at transcription sites to maintain genome integrity," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    5. Yuxin Huang & Wenjing Li & Tzeh Foo & Jae-Hoon Ji & Bo Wu & Nozomi Tomimatsu & Qingming Fang & Boya Gao & Melissa Long & Jingfei Xu & Rouf Maqbool & Bipasha Mukherjee & Tengyang Ni & Salvador Alejo & , 2024. "DSS1 restrains BRCA2’s engagement with dsDNA for homologous recombination, replication fork protection, and R-loop homeostasis," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    6. Zizhi Tang & Ming Zeng & Xiaojun Wang & Chang Guo & Peng Yue & Xiaohu Zhang & Huiqiang Lou & Jun Chen & Dezhi Mu & Daochun Kong & Antony M. Carr & Cong Liu, 2022. "Synthetic lethality between TP53 and ENDOD1," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    7. Samuel D. Chauvin & Shoichiro Ando & Joe A. Holley & Atsushi Sugie & Fang R. Zhao & Subhajit Poddar & Rei Kato & Cathrine A. Miner & Yohei Nitta & Siddharth R. Krishnamurthy & Rie Saito & Yue Ning & Y, 2024. "Inherited C-terminal TREX1 variants disrupt homology-directed repair to cause senescence and DNA damage phenotypes in Drosophila, mice, and humans," Nature Communications, Nature, vol. 15(1), pages 1-23, December.
    8. Arindam Datta & Kajal Biswas & Joshua A. Sommers & Haley Thompson & Sanket Awate & Claudia M. Nicolae & Tanay Thakar & George-Lucian Moldovan & Robert H. Shoemaker & Shyam K. Sharan & Robert M. Brosh, 2021. "WRN helicase safeguards deprotected replication forks in BRCA2-mutated cancer cells," Nature Communications, Nature, vol. 12(1), pages 1-22, December.
    9. Meng Wang & Satoshi Fukushima & Yi-Shuan Sheen & Egle Ramelyte & Noel Cruz-Pacheco & Chenxu Shi & Shanshan Liu & Ishani Banik & Jamie D. Aquino & Martin Sangueza Acosta & Mitchell Levesque & Reinhard , 2024. "The genetic evolution of acral melanoma," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    10. Jun Dai & Shuyu Zheng & Matías M. Falco & Jie Bao & Johanna Eriksson & Sanna Pikkusaari & Sofia Forstén & Jing Jiang & Wenyu Wang & Luping Gao & Fernando Perez-Villatoro & Olli Dufva & Khalid Saeed & , 2024. "Tracing back primed resistance in cancer via sister cells," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    11. Youngho Kwon & Heike Rösner & Weixing Zhao & Platon Selemenakis & Zhuoling He & Ajinkya S. Kawale & Jeffrey N. Katz & Cody M. Rogers & Francisco E. Neal & Aida Badamchi Shabestari & Valdemaras Petrosi, 2023. "DNA binding and RAD51 engagement by the BRCA2 C-terminus orchestrate DNA repair and replication fork preservation," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    12. 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.
    13. Yonina R. Murciano-Goroff & Alison M. Schram & Ezra Y. Rosen & Helen Won & Yixiao Gong & Anne Marie Noronha & Yelena Y. Janjigian & Zsofia K. Stadler & Jason C. Chang & Soo-Ryum Yang & Diana Mandelker, 2022. "Reversion mutations in germline BRCA1/2-mutant tumors reveal a BRCA-mediated phenotype in non-canonical histologies," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    14. Sumin Feng & Sai Ma & Kejiao Li & Shengxian Gao & Shaokai Ning & Jinfeng Shang & Ruiyuan Guo & Yingying Chen & Britny Blumenfeld & Itamar Simon & Qing Li & Rong Guo & Dongyi Xu, 2022. "RIF1-ASF1-mediated high-order chromatin structure safeguards genome integrity," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    15. Ramona N. Moro & Uddipta Biswas & Suhas S. Kharat & Filip D. Duzanic & Prosun Das & Maria Stavrou & Maria C. Raso & Raimundo Freire & Arnab Ray Chaudhuri & Shyam K. Sharan & Lorenza Penengo, 2023. "Interferon restores replication fork stability and cell viability in BRCA-defective cells via ISG15," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    16. Wei Liu & Hongchao Cao & Jing Wang & Areeg Elmusrati & Bing Han & Wei Chen & Ping Zhou & Xiyao Li & Stephen Keysar & Antonio Jimeno & Cun-Yu Wang, 2024. "Histone-methyltransferase KMT2D deficiency impairs the Fanconi anemia/BRCA pathway upon glycolytic inhibition in squamous cell carcinoma," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    17. Domagoj Vugic & Isaac Dumoulin & Charlotte Martin & Anna Minello & Lucia Alvaro-Aranda & Jesus Gomez-Escudero & Rady Chaaban & Rana Lebdy & Catharina Nicolai & Virginie Boucherit & Cyril Ribeyre & Ang, 2023. "Replication gap suppression depends on the double-strand DNA binding activity of BRCA2," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    18. Martina Minoli & Thomas Cantore & Daniel Hanhart & Mirjam Kiener & Tarcisio Fedrizzi & Federico La Manna & Sofia Karkampouna & Panagiotis Chouvardas & Vera Genitsch & Antonio Rodriguez-Calero & Eva Co, 2023. "Bladder cancer organoids as a functional system to model different disease stages and therapy response," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    19. Anne Margriet Heijink & Colin Stok & David Porubsky & Eleni Maria Manolika & Jurrian K. Kanter & Yannick P. Kok & Marieke Everts & H. Rudolf Boer & Anastasia Audrey & Femke J. Bakker & Elles Wierenga , 2022. "Sister chromatid exchanges induced by perturbed replication can form independently of BRCA1, BRCA2 and RAD51," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    20. Zu Ye & Shengfeng Xu & Yin Shi & Xueqian Cheng & Yuan Zhang & Sunetra Roy & Sarita Namjoshi & Michael A. Longo & Todd M. Link & Katharina Schlacher & Guang Peng & Dihua Yu & Bin Wang & John A. Tainer , 2024. "GRB2 stabilizes RAD51 at reversed replication forks suppressing genomic instability and innate immunity against cancer," Nature Communications, Nature, vol. 15(1), pages 1-14, December.

    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:13:y:2022:i:1:d:10.1038_s41467-022-34612-y. 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.