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Circular RNA circTmem241 drives group III innate lymphoid cell differentiation via initiation of Elk3 transcription

Author

Listed:
  • Nian Liu

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

  • Jiacheng He

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

  • Dongdong Fan

    (Chinese Academy of Sciences)

  • Yang Gu

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

  • Jianyi Wang

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

  • Huimu Li

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

  • Xiaoxiao Zhu

    (Chinese Academy of Sciences)

  • Ying Du

    (Chinese Academy of Sciences)

  • Yong Tian

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

  • Benyu Liu

    (Zhengzhou University)

  • Zusen Fan

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

Abstract

Innate lymphoid cells (ILCs) exert important roles in host defense, tissue repair and inflammatory diseases. However, how ILC lineage specification is regulated remains largely elusive. Here we identify that circular RNA circTmem241 is highly expressed in group III innate lymphoid cells (ILC3s) and their progenitor cells. CircTmem241 deficiency impairs ILC3 commitment and attenuates anti-bacterial immunity. Mechanistically, circTmem241 interacts with Nono protein to recruit histone methyltransferase Ash1l onto Elk3 promoter in ILC progenitor cells (ILCPs). Ash1l-mediated histone modifications on Elk3 promoter enhance chromatin accessibility to initiate Elk3 transcription. Of note, circTmem241−/−, Nono−/− and Ash1l−/− ILCPs display impaired ILC3 differentiation, while Elk3 overexpression rescues ILC3 commitment ability. Finally, circTmem241−/−Elk3−/− mice show lower numbers of ILC3s and are more susceptible to bacterial infection. We reveal that the circTmem241-Nono-Ash1l-Elk3 axis is required for the ILCP differentiation into ILC3P and ILC3 maturation, which is important to manipulate this axis for ILC development on treatment of infectious diseases.

Suggested Citation

  • Nian Liu & Jiacheng He & Dongdong Fan & Yang Gu & Jianyi Wang & Huimu Li & Xiaoxiao Zhu & Ying Du & Yong Tian & Benyu Liu & Zusen Fan, 2022. "Circular RNA circTmem241 drives group III innate lymphoid cell differentiation via initiation of Elk3 transcription," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-32322-z
    DOI: 10.1038/s41467-022-32322-z
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    References listed on IDEAS

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    1. Michael G. Constantinides & Benjamin D. McDonald & Philip A. Verhoef & Albert Bendelac, 2014. "A committed precursor to innate lymphoid cells," Nature, Nature, vol. 508(7496), pages 397-401, April.
    2. Chun-Ying Yu & Tung-Cheng Li & Yi-Ying Wu & Chan-Hsien Yeh & Wei Chiang & Ching-Yu Chuang & Hung-Chih Kuo, 2017. "The circular RNA circBIRC6 participates in the molecular circuitry controlling human pluripotency," Nature Communications, Nature, vol. 8(1), pages 1-15, December.
    3. Benyu Liu & Buqing Ye & Xiaoxiao Zhu & Liuliu Yang & Huimu Li & Nian Liu & Pingping Zhu & Tiankun Lu & Luyun He & Yong Tian & Zusen Fan, 2020. "An inducible circular RNA circKcnt2 inhibits ILC3 activation to facilitate colitis resolution," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    4. David Artis & Hergen Spits, 2015. "The biology of innate lymphoid cells," Nature, Nature, vol. 517(7534), pages 293-301, January.
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    Cited by:

    1. Xusheng Zhang & Xintong Gao & Zhen Liu & Fei Shao & Dou Yu & Min Zhao & Xiwen Qin & Shuo Wang, 2024. "Microbiota regulates the TET1-mediated DNA hydroxymethylation program in innate lymphoid cell differentiation," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    2. Wenjuan Zhang & Bowei Zhou & Xiao Yang & Jin Zhao & Jingjuan Hu & Yuqi Ding & Shuteng Zhan & Yifeng Yang & Jun Chen & Fu Zhang & Bingcheng Zhao & Fan Deng & Zebin Lin & Qishun Sun & Fangling Zhang & Z, 2023. "Exosomal circEZH2_005, an intestinal injury biomarker, alleviates intestinal ischemia/reperfusion injury by mediating Gprc5a signaling," Nature Communications, Nature, vol. 14(1), pages 1-17, December.

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