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LncRNA INHEG promotes glioma stem cell maintenance and tumorigenicity through regulating rRNA 2’-O-methylation

Author

Listed:
  • Lihui Liu

    (Chinese Academy of Sciences)

  • Ziyang Liu

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Qinghua Liu

    (Chinese Academy of Sciences)

  • Wei Wu

    (Chinese Academy of Sciences)

  • Peng Lin

    (Westlake University
    Westlake Laboratory of Life Sciences and Biomedicine)

  • Xing Liu

    (Beijing Neurosurgical Institute)

  • Yuechuan Zhang

    (Peking Union Medical College Hospital)

  • Dongpeng Wang

    (Chinese Academy of Sciences)

  • Briana C. Prager

    (Case Western Reserve University
    Case Western Reserve University)

  • Ryan C. Gimple

    (Case Western Reserve University)

  • Jichuan Yu

    (Westlake University
    Westlake Laboratory of Life Sciences and Biomedicine)

  • Weixi Zhao

    (Westlake University
    Westlake Laboratory of Life Sciences and Biomedicine)

  • Qiulian Wu

    (University of Pittsburgh Medical Center)

  • Wei Zhang

    (Capital Medical University)

  • Erzhong Wu

    (Chinese Academy of Sciences)

  • Xiaomin Chen

    (Chinese Academy of Sciences)

  • Jianjun Luo

    (Chinese Academy of Sciences)

  • Jeremy N. Rich

    (University of Pittsburgh Medical Center)

  • Qi Xie

    (Westlake University
    Westlake Laboratory of Life Sciences and Biomedicine)

  • Tao Jiang

    (Beijing Neurosurgical Institute
    Capital Medical University)

  • Runsheng Chen

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

Abstract

Glioblastoma (GBM) ranks among the most lethal of human cancers, containing glioma stem cells (GSCs) that display therapeutic resistance. Here, we report that the lncRNA INHEG is highly expressed in GSCs compared to differentiated glioma cells (DGCs) and promotes GSC self-renewal and tumorigenicity through control of rRNA 2’-O-methylation. INHEG induces the interaction between SUMO2 E3 ligase TAF15 and NOP58, a core component of snoRNP that guides rRNA methylation, to regulate NOP58 sumoylation and accelerate the C/D box snoRNP assembly. INHEG activation enhances rRNA 2’-O-methylation, thereby increasing the expression of oncogenic proteins including EGFR, IGF1R, CDK6 and PDGFRB in glioma cells. Taken together, this study identifies a lncRNA that connects snoRNP-guided rRNA 2’-O-methylation to upregulated protein translation in GSCs, supporting an axis for potential therapeutic targeting of gliomas.

Suggested Citation

  • Lihui Liu & Ziyang Liu & Qinghua Liu & Wei Wu & Peng Lin & Xing Liu & Yuechuan Zhang & Dongpeng Wang & Briana C. Prager & Ryan C. Gimple & Jichuan Yu & Weixi Zhao & Qiulian Wu & Wei Zhang & Erzhong Wu, 2023. "LncRNA INHEG promotes glioma stem cell maintenance and tumorigenicity through regulating rRNA 2’-O-methylation," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43113-5
    DOI: 10.1038/s41467-023-43113-5
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    References listed on IDEAS

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    1. Markus Kretz & Zurab Siprashvili & Ci Chu & Dan E. Webster & Ashley Zehnder & Kun Qu & Carolyn S. Lee & Ross J. Flockhart & Abigail F. Groff & Jennifer Chow & Danielle Johnston & Grace E. Kim & Robert, 2013. "Control of somatic tissue differentiation by the long non-coding RNA TINCR," Nature, Nature, vol. 493(7431), pages 231-235, January.
    2. Mitchell Guttman & John L. Rinn, 2012. "Modular regulatory principles of large non-coding RNAs," Nature, Nature, vol. 482(7385), pages 339-346, February.
    3. Jian Chen & Yanjiao Li & Tzong-Shiue Yu & Renée M. McKay & Dennis K. Burns & Steven G. Kernie & Luis F. Parada, 2012. "A restricted cell population propagates glioblastoma growth after chemotherapy," Nature, Nature, vol. 488(7412), pages 522-526, August.
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