IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-40846-1.html
   My bibliography  Save this article

NFIB facilitates replication licensing by acting as a genome organizer

Author

Listed:
  • Wenting Zhang

    (Peking University Health Science Center)

  • Yue Wang

    (Peking University Health Science Center
    Hangzhou Normal University)

  • Yongjie Liu

    (University of Chinese Academy of Sciences)

  • Cuifang Liu

    (Chinese Academy of Sciences)

  • Yizhou Wang

    (Chinese Academy of Sciences)

  • Lin He

    (Peking University Health Science Center)

  • Xiao Cheng

    (Peking University Health Science Center)

  • Yani Peng

    (Peking University Health Science Center)

  • Lu Xia

    (Peking University Health Science Center)

  • Xiaodi Wu

    (Capital Medical University)

  • Jiajing Wu

    (Capital Medical University)

  • Yu Zhang

    (Peking University Health Science Center)

  • Luyang Sun

    (Peking University Health Science Center)

  • Ping Chen

    (Capital Medical University)

  • Guohong Li

    (Chinese Academy of Sciences)

  • Qiang Tu

    (University of Chinese Academy of Sciences)

  • Jing Liang

    (Peking University Health Science Center)

  • Yongfeng Shang

    (Peking University Health Science Center
    Hangzhou Normal University)

Abstract

The chromatin-based rule governing the selection and activation of replication origins in metazoans remains to be investigated. Here we report that NFIB, a member of Nuclear Factor I (NFI) family that was initially purified in host cells to promote adenoviral DNA replication but has since mainly been investigated in transcription regulation, is physically associated with the pre-replication complex (pre-RC) in mammalian cells. Genomic analyses reveal that NFIB facilitates the assembly of the pre-RC by increasing chromatin accessibility. Nucleosome binding and single-molecule magnetic tweezers shows that NFIB binds to and opens up nucleosomes. Transmission electron microscopy indicates that NFIB promotes nucleosome eviction on parental chromatin. NFIB deficiency leads to alterations of chromosome contacts/compartments in both G1 and S phase and affects the firing of a subset of origins at early-replication domains. Significantly, cancer-associated NFIB overexpression provokes gene duplication and genomic alterations recapitulating the genetic aberrance in clinical breast cancer and empowering cancer cells to dynamically evolve growth advantage and drug resistance. Together, these results point a role for NFIB in facilitating replication licensing by acting as a genome organizer, shedding new lights on the biological function of NFIB and on the replication origin selection in eukaryotes.

Suggested Citation

  • Wenting Zhang & Yue Wang & Yongjie Liu & Cuifang Liu & Yizhou Wang & Lin He & Xiao Cheng & Yani Peng & Lu Xia & Xiaodi Wu & Jiajing Wu & Yu Zhang & Luyang Sun & Ping Chen & Guohong Li & Qiang Tu & Jin, 2023. "NFIB facilitates replication licensing by acting as a genome organizer," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40846-1
    DOI: 10.1038/s41467-023-40846-1
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-40846-1
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-40846-1?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. Yilong Li & Nicola D. Roberts & Jeremiah A. Wala & Ofer Shapira & Steven E. Schumacher & Kiran Kumar & Ekta Khurana & Sebastian Waszak & Jan O. Korbel & James E. Haber & Marcin Imielinski & Joachim We, 2020. "Patterns of somatic structural variation in human cancer genomes," Nature, Nature, vol. 578(7793), pages 112-121, February.
    2. Nataliya Petryk & Malik Kahli & Yves d'Aubenton-Carafa & Yan Jaszczyszyn & Yimin Shen & Maud Silvain & Claude Thermes & Chun-Long Chen & Olivier Hyrien, 2016. "Replication landscape of the human genome," Nature Communications, Nature, vol. 7(1), pages 1-13, April.
    3. David Dominguez-Sola & Carol Y. Ying & Carla Grandori & Luca Ruggiero & Brenden Chen & Muyang Li & Denise A. Galloway & Wei Gu & Jean Gautier & Riccardo Dalla-Favera, 2007. "Non-transcriptional control of DNA replication by c-Myc," Nature, Nature, vol. 448(7152), pages 445-451, July.
    4. Haizhen Long & Liwei Zhang & Mengjie Lv & Zengqi Wen & Wenhao Zhang & Xiulan Chen & Peitao Zhang & Tongqing Li & Luyuan Chang & Caiwei Jin & Guozhao Wu & Xi Wang & Fuquan Yang & Jianfeng Pei & Ping Ch, 2020. "H2A.Z facilitates licensing and activation of early replication origins," Nature, Nature, vol. 577(7791), pages 576-581, January.
    5. Huijian Wu & Yupeng Chen & Jing Liang & Bin Shi & Ge Wu & Ying Zhang & Dan Wang & Ruifang Li & Xia Yi & Hua Zhang & Luyang Sun & Yongfeng Shang, 2005. "Hypomethylation-linked activation of PAX2 mediates tamoxifen-stimulated endometrial carcinogenesis," Nature, Nature, vol. 438(7070), pages 981-987, December.
    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. Eri Koyanagi & Yoko Kakimoto & Tamiko Minamisawa & Fumiya Yoshifuji & Toyoaki Natsume & Atsushi Higashitani & Tomoo Ogi & Antony M. Carr & Masato T. Kanemaki & Yasukazu Daigaku, 2022. "Global landscape of replicative DNA polymerase usage in the human genome," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    2. Michelle Dietzen & Haoran Zhai & Olivia Lucas & Oriol Pich & Christopher Barrington & Wei-Ting Lu & Sophia Ward & Yanping Guo & Robert E. Hynds & Simone Zaccaria & Charles Swanton & Nicholas McGranaha, 2024. "Replication timing alterations are associated with mutation acquisition during breast and lung cancer evolution," Nature Communications, Nature, vol. 15(1), pages 1-23, December.
    3. Richard Nisa, 2015. "Capturing humanitarian war: the collusion of violence and care in US-managed military detention," Environment and Planning A, , vol. 47(11), pages 2276-2291, November.
    4. Yasuhiko Haga & Yoshitaka Sakamoto & Keiko Kajiya & Hitomi Kawai & Miho Oka & Noriko Motoi & Masayuki Shirasawa & Masaya Yotsukura & Shun-Ichi Watanabe & Miyuki Arai & Junko Zenkoh & Kouya Shiraishi &, 2023. "Whole-genome sequencing reveals the molecular implications of the stepwise progression of lung adenocarcinoma," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    5. Liyuan Zhou & Qiongzi Qiu & Qing Zhou & Jianwei Li & Mengqian Yu & Kezhen Li & Lingling Xu & Xiaohui Ke & Haiming Xu & Bingjian Lu & Hui Wang & Weiguo Lu & Pengyuan Liu & Yan Lu, 2022. "Long-read sequencing unveils high-resolution HPV integration and its oncogenic progression in cervical cancer," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    6. Aina Maria Mas & Enrique Goñi & Igor Ruiz de los Mozos & Aida Arcas & Luisa Statello & Jovanna González & Lorea Blázquez & Wei Ting Chelsea Lee & Dipika Gupta & Álvaro Sejas & Shoko Hoshina & Alexandr, 2023. "ORC1 binds to cis-transcribed RNAs for efficient activation of replication origins," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    7. Adam C. Weiner & Marc J. Williams & Hongyu Shi & Ignacio Vázquez-García & Sohrab Salehi & Nicole Rusk & Samuel Aparicio & Sohrab P. Shah & Andrew McPherson, 2024. "Inferring replication timing and proliferation dynamics from single-cell DNA sequencing data," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    8. Yu Chen & Amy Y. Wang & Courtney A. Barkley & Yixin Zhang & Xinyang Zhao & Min Gao & Mick D. Edmonds & Zechen Chong, 2023. "Deciphering the exact breakpoints of structural variations using long sequencing reads with DeBreak," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    9. Jinhyun Kim & Sungsik Kim & Huiran Yeom & Seo Woo Song & Kyoungseob Shin & Sangwook Bae & Han Suk Ryu & Ji Young Kim & Ahyoun Choi & Sumin Lee & Taehoon Ryu & Yeongjae Choi & Hamin Kim & Okju Kim & Yu, 2023. "Barcoded multiple displacement amplification for high coverage sequencing in spatial genomics," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    10. Congcong Tian & Jiaqi Zhou & Xinran Li & Yuan Gao & Qing Wen & Xing Kang & Nan Wang & Yuan Yao & Jiuhang Jiang & Guibing Song & Tianjun Zhang & Suili Hu & JingYi Liao & Chuanhe Yu & Zhiquan Wang & Xia, 2023. "Impaired histone inheritance promotes tumor progression," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    11. Alexander Martinez-Fundichely & Austin Dixon & Ekta Khurana, 2022. "Modeling tissue-specific breakpoint proximity of structural variations from whole-genomes to identify cancer drivers," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    12. Anastasiya Kishkevich & Sanjeeta Tamang & Michael O. Nguyen & Judith Oehler & Elena Bulmaga & Christos Andreadis & Carl A. Morrow & Manisha Jalan & Fekret Osman & Matthew C. Whitby, 2022. "Rad52’s DNA annealing activity drives template switching associated with restarted DNA replication," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    13. Yi-Li Feng & Qian Liu & Ruo-Dan Chen & Si-Cheng Liu & Zhi-Cheng Huang & Kun-Ming Liu & Xiao-Ying Yang & An-Yong Xie, 2022. "DNA nicks induce mutational signatures associated with BRCA1 deficiency," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    14. Manisha Jalan & Aman Sharma & Xin Pei & Nils Weinhold & Erika S. Buechelmaier & Yingjie Zhu & Sana Ahmed-Seghir & Abhirami Ratnakumar & Melody Bona & Niamh McDermott & Joan Gomez-Aguilar & Kyrie S. An, 2024. "RAD52 resolves transcription-replication conflicts to mitigate R-loop induced genome instability," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    15. Judith Oehler & Carl A. Morrow & Matthew C. Whitby, 2023. "Gene duplication and deletion caused by over-replication at a fork barrier," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    16. Laura Curti & Sara Rohban & Nicola Bianchi & Ottavio Croci & Adrian Andronache & Sara Barozzi & Michela Mattioli & Fernanda Ricci & Elena Pastori & Silvia Sberna & Simone Bellotti & Anna Accialini & R, 2024. "CDK12 controls transcription at damaged genes and prevents MYC-induced transcription-replication conflicts," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    17. Chunyang Bao & Richard W. Tourdot & Gregory J. Brunette & Chip Stewart & Lili Sun & Hideo Baba & Masayuki Watanabe & Agoston T. Agoston & Kunal Jajoo & Jon M. Davison & Katie S. Nason & Gad Getz & Ken, 2023. "Genomic signatures of past and present chromosomal instability in Barrett’s esophagus and early esophageal adenocarcinoma," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    18. Luan Nguyen & Arne Hoeck & Edwin Cuppen, 2022. "Machine learning-based tissue of origin classification for cancer of unknown primary diagnostics using genome-wide mutation features," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    19. Eva G. Álvarez & Jonas Demeulemeester & Paula Otero & Clemency Jolly & Daniel García-Souto & Ana Pequeño-Valtierra & Jorge Zamora & Marta Tojo & Javier Temes & Adrian Baez-Ortega & Bernardo Rodriguez-, 2021. "Aberrant integration of Hepatitis B virus DNA promotes major restructuring of human hepatocellular carcinoma genome architecture," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    20. Stefano Gnan & Joseph M. Josephides & Xia Wu & Manuela Spagnuolo & Dalila Saulebekova & Mylène Bohec & Marie Dumont & Laura G. Baudrin & Daniele Fachinetti & Sylvain Baulande & Chun-Long Chen, 2022. "Kronos scRT: a uniform framework for single-cell replication timing analysis," Nature Communications, Nature, vol. 13(1), pages 1-15, 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:14:y:2023:i:1:d:10.1038_s41467-023-40846-1. 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.