IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-51634-w.html
   My bibliography  Save this article

IGF2BP3 promotes mRNA degradation through internal m7G modification

Author

Listed:
  • Chang Liu

    (The University of Chicago
    The University of Chicago
    Stanford University)

  • Xiaoyang Dou

    (The University of Chicago
    The University of Chicago)

  • Yutao Zhao

    (The University of Chicago
    The University of Chicago)

  • Linda Zhang

    (The University of Chicago
    The University of Chicago)

  • Lisheng Zhang

    (The University of Chicago
    The University of Chicago
    The Hong Kong University of Science and Technology
    The Hong Kong University of Science and Technology)

  • Qing Dai

    (The University of Chicago
    The University of Chicago)

  • Jun Liu

    (Peking University
    Peking University)

  • Tong Wu

    (The University of Chicago
    The University of Chicago)

  • Yu Xiao

    (The University of Chicago
    The University of Chicago)

  • Chuan He

    (The University of Chicago
    The University of Chicago)

Abstract

Recent studies have suggested that mRNA internal m7G and its writer protein METTL1 are closely related to cell metabolism and cancer regulation. Here, we identify that IGF2BP family proteins IGF2BP1-3 can preferentially bind internal mRNA m7G. Such interactions, especially IGF2BP3 with m7G, could promote the degradation of m7G target transcripts in cancer cells. IGF2BP3 is more responsive to changes of m7G modification, while IGF2BP1 prefers m6A to stabilize the bound transcripts. We also demonstrate that p53 transcript, TP53, is m7G-modified at its 3’UTR in cancer cells. In glioblastoma, the methylation level and the half lifetime of the modified transcript could be modulated by tuning IGF2BP3, or by site-specific targeting of m7G through a dCas13b-guided system, resulting in modulation of cancer progression and chemosensitivity.

Suggested Citation

  • Chang Liu & Xiaoyang Dou & Yutao Zhao & Linda Zhang & Lisheng Zhang & Qing Dai & Jun Liu & Tong Wu & Yu Xiao & Chuan He, 2024. "IGF2BP3 promotes mRNA degradation through internal m7G modification," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51634-w
    DOI: 10.1038/s41467-024-51634-w
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-51634-w
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-51634-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. Jeetayu Biswas & Vivek L. Patel & Varun Bhaskar & Jeffrey A. Chao & Robert H. Singer & Carolina Eliscovich, 2019. "The structural basis for RNA selectivity by the IMP family of RNA-binding proteins," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
    2. Xiao Wang & Zhike Lu & Adrian Gomez & Gary C. Hon & Yanan Yue & Dali Han & Ye Fu & Marc Parisien & Qing Dai & Guifang Jia & Bing Ren & Tao Pan & Chuan He, 2014. "N6-methyladenosine-dependent regulation of messenger RNA stability," Nature, Nature, vol. 505(7481), pages 117-120, January.
    3. Wenqi Xu & Jiahui Li & Chenxi He & Jing Wen & Honghui Ma & Bowen Rong & Jianbo Diao & Liyong Wang & Jiahua Wang & Feizhen Wu & Li Tan & Yujiang Geno Shi & Yang Shi & Hongjie Shen, 2021. "METTL3 regulates heterochromatin in mouse embryonic stem cells," Nature, Nature, vol. 591(7849), pages 317-321, March.
    4. Tim Schneider & Lee-Hsueh Hung & Masood Aziz & Anna Wilmen & Stephanie Thaum & Jacqueline Wagner & Robert Janowski & Simon Müller & Silke Schreiner & Peter Friedhoff & Stefan Hüttelmaier & Dierk Niess, 2019. "Combinatorial recognition of clustered RNA elements by the multidomain RNA-binding protein IMP3," Nature Communications, Nature, vol. 10(1), pages 1-18, 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. Yan Xu & Zhuowei Zhou & Xinmei Kang & Lijie Pan & Chang Liu & Xiaoqi Liang & Jiajie Chu & Shuai Dong & Yanli Li & Qiuli Liu & Yuetong Sun & Shanshan Yu & Qi Zhang, 2022. "Mettl3-mediated mRNA m6A modification controls postnatal liver development by modulating the transcription factor Hnf4a," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    2. Xin Yang & Robinson Triboulet & Qi Liu & Erdem Sendinc & Richard I. Gregory, 2022. "Exon junction complex shapes the m6A epitranscriptome," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    3. Shujie Chen, & Lu Zhang & Mengjie Li & Ying Zhang & Meng Sun & Lingfang Wang & Jiebo Lin & Yun Cui & Qian Chen & Chenqi Jin & Xiang Li & Boya Wang & Hao Chen & Tianhua Zhou & Liangjing Wang & Chih-Hun, 2022. "Fusobacterium nucleatum reduces METTL3-mediated m6A modification and contributes to colorectal cancer metastasis," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    4. Zhiyuan Luo & Jiacheng Zhang & Jingyi Fei & Shengdong Ke, 2022. "Deep learning modeling m6A deposition reveals the importance of downstream cis-element sequences," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    5. Xiao Han & Lijuan Liu & Saihua Huang & Wenfeng Xiao & Yajing Gao & Weitao Zhou & Caiyan Zhang & Hongmei Zheng & Lan Yang & Xueru Xie & Qiuyan Liang & Zikun Tu & Hongmiao Yu & Jinrong Fu & Libo Wang & , 2023. "RNA m6A methylation modulates airway inflammation in allergic asthma via PTX3-dependent macrophage homeostasis," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    6. Sakshi Jain & Lukasz Koziej & Panagiotis Poulis & Igor Kaczmarczyk & Monika Gaik & Michal Rawski & Namit Ranjan & Sebastian Glatt & Marina V. Rodnina, 2023. "Modulation of translational decoding by m6A modification of mRNA," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    7. Bin Li & Wen Xi & Ying Bai & Xue Liu & Yuan Zhang & Lu Li & Liang Bian & Chenchen Liu & Ying Tang & Ling Shen & Li Yang & Xiaochun Gu & Jian Xie & Zhongqiu Zhou & Yu Wang & Xiaoyu Yu & Jianhong Wang &, 2023. "FTO-dependent m6A modification of Plpp3 in circSCMH1-regulated vascular repair and functional recovery following stroke," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    8. Xuan Ye & Wen Yang & Soon Yi & Yanan Zhao & Gabriele Varani & Eckhard Jankowsky & Fan Yang, 2023. "Two distinct binding modes provide the RNA-binding protein RbFox with extraordinary sequence specificity," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    9. Hyun Jung Hwang & Hongseok Ha & Ban Seok Lee & Bong Heon Kim & Hyun Kyu Song & Yoon Ki Kim, 2022. "LC3B is an RNA-binding protein to trigger rapid mRNA degradation during autophagy," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    10. Christopher P. Watkins & Wen Zhang & Adam C. Wylder & Christopher D. Katanski & Tao Pan, 2022. "A multiplex platform for small RNA sequencing elucidates multifaceted tRNA stress response and translational regulation," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    11. Guoqiang Zhang & Yongru Xu & Xiaona Wang & Yuanxiang Zhu & Liangliang Wang & Wenxin Zhang & Yiru Wang & Yajie Gao & Xuna Wu & Ying Cheng & Qinmiao Sun & Dahua Chen, 2022. "Dynamic FMR1 granule phase switch instructed by m6A modification contributes to maternal RNA decay," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    12. Xiaojie Ma & Jie Cao & Ziyu Zhou & Yunkun Lu & Qin Li & Yan Jin & Guo Chen & Weiyun Wang & Wenyan Ge & Xi Chen & Zhensheng Hu & Xiao Shu & Qian Deng & Jiaqi Pu & Chengzhen Liang & Junfen Fu & Jianzhao, 2022. "N6-methyladenosine modification-mediated mRNA metabolism is essential for human pancreatic lineage specification and islet organogenesis," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    13. Man Zhang & Yunping Zeng & Rong Peng & Jie Dong & Yelin Lan & Sujuan Duan & Zhenyi Chang & Jian Ren & Guanzheng Luo & Bing Liu & Kamil Růžička & Kewei Zhao & Hong-Bin Wang & Hong-Lei Jin, 2022. "N6-methyladenosine RNA modification regulates photosynthesis during photodamage in plants," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    14. Xiangbin Ruan & Kaining Hu & Xiaochang Zhang, 2023. "PIE-seq: identifying RNA-binding protein targets by dual RNA-deaminase editing and sequencing," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    15. Valter Bergant & Daniel Schnepf & Niklas Andrade Krätzig & Philipp Hubel & Christian Urban & Thomas Engleitner & Ronald Dijkman & Bernhard Ryffel & Katja Steiger & Percy A. Knolle & Georg Kochs & Rola, 2023. "mRNA 3’UTR lengthening by alternative polyadenylation attenuates inflammatory responses and correlates with virulence of Influenza A virus," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    16. Mwikali Kioko & Alena Pance & Shaban Mwangi & David Goulding & Alison Kemp & Martin Rono & Lynette Isabella Ochola-Oyier & Pete C. Bull & Philip Bejon & Julian C. Rayner & Abdirahman I. Abdi, 2023. "Extracellular vesicles could be a putative posttranscriptional regulatory mechanism that shapes intracellular RNA levels in Plasmodium falciparum," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    17. Yichi Niu & Jiayi Luo & Chenghang Zong, 2024. "Single-cell total-RNA profiling unveils regulatory hubs of transcription factors," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    18. Christopher J. Gilbert & Charles P. Rabolli & Volha A. Golubeva & Kristina M. Sattler & Meifang Wang & Arsh Ketabforoush & W. David Arnold & Christoph Lepper & Federica Accornero, 2024. "YTHDF2 governs muscle size through a targeted modulation of proteostasis," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    19. An Xu & Mo Liu & Mo-Fan Huang & Yang Zhang & Ruifeng Hu & Julian A. Gingold & Ying Liu & Dandan Zhu & Chian-Shiu Chien & Wei-Chen Wang & Zian Liao & Fei Yuan & Chih-Wei Hsu & Jian Tu & Yao Yu & Taylor, 2023. "Rewired m6A epitranscriptomic networks link mutant p53 to neoplastic transformation," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    20. Sujun Yan & Xiaoling Zhou & Canlan Wu & Yunyi Gao & Yu Qian & Jingyu Hou & Renxiang Xie & Bing Han & Zhanghui Chen & Saisai Wei & Xiangwei Gao, 2023. "Adipocyte YTH N(6)-methyladenosine RNA-binding protein 1 protects against obesity by promoting white adipose tissue beiging in male mice," Nature Communications, Nature, vol. 14(1), pages 1-13, 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:15:y:2024:i:1:d:10.1038_s41467-024-51634-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.