IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-32322-z.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-32322-z
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-32322-z?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. 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.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    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.

    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. Panpan Tian & Wenwen Yang & Xiaowei Guo & Tixiao Wang & Siyu Tan & Renhui Sun & Rong Xiao & Yuzhen Wang & Deyan Jiao & Yachen Xu & Yanfei Wei & Zhuanchang Wu & Chunyang Li & Lifen Gao & Chunhong Ma & , 2023. "Early life gut microbiota sustains liver-resident natural killer cells maturation via the butyrate-IL-18 axis," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    2. Hiroki Furuya & Yosuke Toda & Arifumi Iwata & Mizuki Kanai & Kodai Kato & Takashi Kumagai & Takahiro Kageyama & Shigeru Tanaka & Lisa Fujimura & Akemi Sakamoto & Masahiko Hatano & Akira Suto & Kotaro , 2024. "Stage-specific GATA3 induction promotes ILC2 development after lineage commitment," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    3. Yuying Huang & Lin Zhu & Shipeng Cheng & Ranran Dai & Chunrong Huang & Yanyan Song & Bo Peng & Xuezhen Li & Jing Wen & Yi Gong & Yunqian Hu & Ling Qian & Linyun Zhu & Fengying Zhang & Li Yu & Chunyan , 2023. "Solar ultraviolet B radiation promotes α-MSH secretion to attenuate the function of ILC2s via the pituitary–lung axis," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    4. Wanying Wu & Jinyang Zhang & Xiaofei Cao & Zhengyi Cai & Fangqing Zhao, 2022. "Exploring the cellular landscape of circular RNAs using full-length single-cell RNA sequencing," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    5. Bertha Estrella & Elena N. Naumova & Magda Cepeda & Trudy Voortman & Peter D. Katsikis & Hemmo A. Drexhage, 2019. "Effects of Air Pollution on Lung Innate Lymphoid Cells: Review of In Vitro and In Vivo Experimental Studies," IJERPH, MDPI, vol. 16(13), pages 1-15, July.
    6. Zhe Gong & Jinjin Zhu & Junxin Chen & Fan Feng & Haitao Zhang & Zheyuan Zhang & Chenxin Song & Kaiyu Liang & Shuhui Yang & Shunwu Fan & Xiangqian Fang & Shuying Shen, 2023. "CircRREB1 mediates lipid metabolism related senescent phenotypes in chondrocytes through FASN post-translational modifications," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    7. 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.
    8. Jana H. Badrani & Allyssa N. Strohm & Lee Lacasa & Blake Civello & Kellen Cavagnero & Yung-An Haung & Michael Amadeo & Luay H. Naji & Sean J. Lund & Anthea Leng & Hyojoung Kim & Rachel E. Baum & Nasee, 2022. "RNA-binding protein RBM3 intrinsically suppresses lung innate lymphoid cell activation and inflammation partially through CysLT1R," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    9. Zhenzhen Chen & Qiankun He & Tiankun Lu & Jiayi Wu & Gaoli Shi & Luyun He & Hong Zong & Benyu Liu & Pingping Zhu, 2023. "mcPGK1-dependent mitochondrial import of PGK1 promotes metabolic reprogramming and self-renewal of liver TICs," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    10. Vaishnavi Nimbalkar & Manish Kamble & Jagdish Baheti, 2020. "In-Vitro Assay to Investigate the Anti-Inflammatory Activity of Hydroalcoholic Leaves Extract of Acacia Auriculiformis A.Cunn. Ex Benth," International Journal of Research and Scientific Innovation, International Journal of Research and Scientific Innovation (IJRSI), vol. 7(4), pages 07-09, April.
    11. Hung-Wei Cheng & Urs Mörbe & Mechthild Lütge & Céline Engetschwiler & Lucas Onder & Mario Novkovic & Cristina Gil-Cruz & Christian Perez-Shibayama & Thomas Hehlgans & Elke Scandella & Burkhard Ludewig, 2022. "Intestinal fibroblastic reticular cell niches control innate lymphoid cell homeostasis and function," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    12. Min Zhao & Fei Shao & Dou Yu & Jiaqi Zhang & Zhen Liu & Jiangwen Ma & Pengyan Xia & Shuo Wang, 2022. "Maturation and specialization of group 2 innate lymphoid cells through the lung-gut axis," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    13. Paula A. Clark & Mayuri Gogoi & Noe Rodriguez-Rodriguez & Ana C. F. Ferreira & Jane E. Murphy & Jennifer A. Walker & Alastair Crisp & Helen E. Jolin & Jacqueline D. Shields & Andrew N. J. McKenzie, 2024. "Recipient tissue microenvironment determines developmental path of intestinal innate lymphoid progenitors," Nature Communications, Nature, vol. 15(1), pages 1-17, 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:13:y:2022:i:1:d:10.1038_s41467-022-32322-z. 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.