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. 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.
    2. 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.
    3. 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.
    4. 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.
    5. 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.
    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. 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.
    3. 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.
    4. 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.
    5. 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.
    6. 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.
    7. 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.
    8. 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.
    9. 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.
    10. 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.
    11. Yoshitaka Sakamoto & Shuhei Miyake & Miho Oka & Akinori Kanai & Yosuke Kawai & Satoi Nagasawa & Yuichi Shiraishi & Katsushi Tokunaga & Takashi Kohno & Masahide Seki & Yutaka Suzuki & Ayako Suzuki, 2022. "Phasing analysis of lung cancer genomes using a long read sequencer," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    12. Yoshihisa Kobayashi & Geoffrey R. Oxnard & Elizabeth F. Cohen & Navin R. Mahadevan & Joao V. Alessi & Yin P. Hung & Arrien A. Bertram & David E. Heppner & Mauricio F. Ribeiro & Karina P. Sacardo & Rod, 2022. "Genomic and biological study of fusion genes as resistance mechanisms to EGFR inhibitors," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    13. Dashiell J. Massey & Amnon Koren, 2022. "High-throughput analysis of single human cells reveals the complex nature of DNA replication timing control," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    14. Zhuoran Xu & Quan Li & Luigi Marchionni & Kai Wang, 2023. "PhenoSV: interpretable phenotype-aware model for the prioritization of genes affected by structural variants," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    15. Heyang Cui & Yong Zhou & Fang Wang & Caixia Cheng & Weimin Zhang & Ruifang Sun & Ling Zhang & Yanghui Bi & Min Guo & Yan Zhou & Xinhui Wang & Jiaxin Ren & Ruibing Bai & Ning Ding & Chen Cheng & Longlo, 2022. "Characterization of somatic structural variations in 528 Chinese individuals with Esophageal squamous cell carcinoma," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    16. Qiliang Ding & Matthew M. Edwards & Ning Wang & Xiang Zhu & Alexa N. Bracci & Michelle L. Hulke & Ya Hu & Yao Tong & Joyce Hsiao & Christine J. Charvet & Sulagna Ghosh & Robert E. Handsaker & Kevin Eg, 2021. "The genetic architecture of DNA replication timing in human pluripotent stem cells," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
    17. Sai Li & Michael R. Wasserman & Olga Yurieva & Lu Bai & Michael E. O’Donnell & Shixin Liu, 2022. "Nucleosome-directed replication origin licensing independent of a consensus DNA sequence," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    18. Kate E. Coleman & Yandong Yin & Sarah Kit Leng Lui & Sarah Keegan & David Fenyo & Duncan J. Smith & Eli Rothenberg & Tony T. Huang, 2022. "USP1-trapping lesions as a source of DNA replication stress and genomic instability," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    19. Lorenzo Corazzi & Vivien S. Ionasz & Sergej Andrejev & Li-Chin Wang & Athanasios Vouzas & Marco Giaisi & Giulia Di Muzio & Boyu Ding & Anna J. M. Marx & Jonas Henkenjohann & Michael M. Allers & David , 2024. "Linear interaction between replication and transcription shapes DNA break dynamics at recurrent DNA break Clusters," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    20. Holger Schwender & Silvia Selinski & Meinolf Blaszkewicz & Rosemarie Marchan & Katja Ickstadt & Klaus Golka & Jan G Hengstler, 2012. "Distinct SNP Combinations Confer Susceptibility to Urinary Bladder Cancer in Smokers and Non-Smokers," PLOS ONE, Public Library of Science, vol. 7(12), pages 1-12, 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.