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m6A in mRNA coding regions promotes translation via the RNA helicase-containing YTHDC2

Author

Listed:
  • Yuanhui Mao

    (Cornell University)

  • Leiming Dong

    (Cornell University)

  • Xiao-Min Liu

    (Cornell University)

  • Jiayin Guo

    (Nanjing Medical University)

  • Honghui Ma

    (Tongji University School of Medicine)

  • Bin Shen

    (Nanjing Medical University)

  • Shu-Bing Qian

    (Cornell University)

Abstract

Dynamic mRNA modification in the form of N6-methyladenosine (m6A) adds considerable richness and sophistication to gene regulation. The m6A mark is asymmetrically distributed along mature mRNAs, with approximately 35% of m6A residues located within the coding region (CDS). It has been suggested that methylation in CDS slows down translation elongation. However, neither the decoding feature of endogenous mRNAs nor the physiological significance of CDS m6A has been clearly defined. Here, we found that CDS m6A leads to ribosome pausing in a codon-specific manner. Unexpectedly, removing CDS m6A from these transcripts results in a further decrease of translation. A systemic analysis of RNA structural datasets revealed that CDS m6A positively regulates translation by resolving mRNA secondary structures. We further demonstrate that the elongation-promoting effect of CDS methylation requires the RNA helicase-containing m6A reader YTHDC2. Our findings established the physiological significance of CDS methylation and uncovered non-overlapping function of m6A reader proteins.

Suggested Citation

  • Yuanhui Mao & Leiming Dong & Xiao-Min Liu & Jiayin Guo & Honghui Ma & Bin Shen & Shu-Bing Qian, 2019. "m6A in mRNA coding regions promotes translation via the RNA helicase-containing YTHDC2," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-019-13317-9
    DOI: 10.1038/s41467-019-13317-9
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    Cited by:

    1. P Acera Mateos & A J Sethi & A Ravindran & A Srivastava & K Woodward & S Mahmud & M Kanchi & M Guarnacci & J Xu & Z W S Yuen & Y Zhou & A Sneddon & W Hamilton & J Gao & L M Starrs & R Hayashi & V Wick, 2024. "Prediction of m6A and m5C at single-molecule resolution reveals a transcriptome-wide co-occurrence of RNA modifications," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    2. Chisa Shiraishi & Akinobu Matsumoto & Kazuya Ichihara & Taishi Yamamoto & Takeshi Yokoyama & Taisuke Mizoo & Atsushi Hatano & Masaki Matsumoto & Yoshikazu Tanaka & Eriko Matsuura-Suzuki & Shintaro Iwa, 2023. "RPL3L-containing ribosomes determine translation elongation dynamics required for cardiac function," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    3. 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.
    4. Huaxia Shi & Ying Xu & Na Tian & Ming Yang & Fu-Sen Liang, 2022. "Inducible and reversible RNA N6-methyladenosine editing," Nature Communications, Nature, vol. 13(1), pages 1-10, December.

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