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The dynamic N1-methyladenosine methylome in eukaryotic messenger RNA

Author

Listed:
  • Dan Dominissini

    (The University of Chicago
    Howard Hughes Medical Institute, The University of Chicago)

  • Sigrid Nachtergaele

    (The University of Chicago
    Howard Hughes Medical Institute, The University of Chicago)

  • Sharon Moshitch-Moshkovitz

    (Cancer Research Center, Chaim Sheba Medical Center)

  • Eyal Peer

    (Cancer Research Center, Chaim Sheba Medical Center
    Sackler School of Medicine, Tel Aviv University)

  • Nitzan Kol

    (Cancer Research Center, Chaim Sheba Medical Center)

  • Moshe Shay Ben-Haim

    (Cancer Research Center, Chaim Sheba Medical Center
    Sackler School of Medicine, Tel Aviv University)

  • Qing Dai

    (The University of Chicago
    Howard Hughes Medical Institute, The University of Chicago)

  • Ayelet Di Segni

    (Cancer Research Center, Chaim Sheba Medical Center)

  • Mali Salmon-Divon

    (Cancer Research Center, Chaim Sheba Medical Center)

  • Wesley C. Clark

    (The University of Chicago)

  • Guanqun Zheng

    (The University of Chicago)

  • Tao Pan

    (The University of Chicago)

  • Oz Solomon

    (Cancer Research Center, Chaim Sheba Medical Center
    The Mina and Everard Goodman Faculty of Life Sciences, Bar-Ilan University)

  • Eran Eyal

    (Cancer Research Center, Chaim Sheba Medical Center)

  • Vera Hershkovitz

    (Cancer Research Center, Chaim Sheba Medical Center)

  • Dali Han

    (The University of Chicago
    Howard Hughes Medical Institute, The University of Chicago)

  • Louis C. Doré

    (The University of Chicago
    Howard Hughes Medical Institute, The University of Chicago)

  • Ninette Amariglio

    (Cancer Research Center, Chaim Sheba Medical Center
    The Mina and Everard Goodman Faculty of Life Sciences, Bar-Ilan University)

  • Gideon Rechavi

    (Cancer Research Center, Chaim Sheba Medical Center
    Sackler School of Medicine, Tel Aviv University)

  • Chuan He

    (The University of Chicago
    Howard Hughes Medical Institute, The University of Chicago
    The University of Chicago)

Abstract

Gene expression can be regulated post-transcriptionally through dynamic and reversible RNA modifications. A recent noteworthy example is N6-methyladenosine (m6A), which affects messenger RNA (mRNA) localization, stability, translation and splicing. Here we report on a new mRNA modification, N1-methyladenosine (m1A), that occurs on thousands of different gene transcripts in eukaryotic cells, from yeast to mammals, at an estimated average transcript stoichiometry of 20% in humans. Employing newly developed sequencing approaches, we show that m1A is enriched around the start codon upstream of the first splice site: it preferentially decorates more structured regions around canonical and alternative translation initiation sites, is dynamic in response to physiological conditions, and correlates positively with protein production. These unique features are highly conserved in mouse and human cells, strongly indicating a functional role for m1A in promoting translation of methylated mRNA.

Suggested Citation

  • Dan Dominissini & Sigrid Nachtergaele & Sharon Moshitch-Moshkovitz & Eyal Peer & Nitzan Kol & Moshe Shay Ben-Haim & Qing Dai & Ayelet Di Segni & Mali Salmon-Divon & Wesley C. Clark & Guanqun Zheng & T, 2016. "The dynamic N1-methyladenosine methylome in eukaryotic messenger RNA," Nature, Nature, vol. 530(7591), pages 441-446, February.
    • Handle: RePEc:nat:nature:v:530:y:2016:i:7591:d:10.1038_nature16998
    DOI: 10.1038/nature16998
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    Citations

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    Cited by:

    1. Moshe Shay Ben-Haim & Yishay Pinto & Sharon Moshitch-Moshkovitz & Vera Hershkovitz & Nitzan Kol & Tammy Diamant-Levi & Michal Schnaider Beeri & Ninette Amariglio & Haim Y. Cohen & Gideon Rechavi, 2021. "Dynamic regulation of N6,2′-O-dimethyladenosine (m6Am) in obesity," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    2. 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.
    3. Zhangli Su & Ida Monshaugen & Briana Wilson & Fengbin Wang & Arne Klungland & Rune Ougland & Anindya Dutta, 2022. "TRMT6/61A-dependent base methylation of tRNA-derived fragments regulates gene-silencing activity and the unfolded protein response in bladder cancer," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    4. Katja Hartstock & Nadine A. Kueck & Petr Spacek & Anna Ovcharenko & Sabine Hüwel & Nicolas V. Cornelissen & Amarnath Bollu & Christoph Dieterich & Andrea Rentmeister, 2023. "MePMe-seq: antibody-free simultaneous m6A and m5C mapping in mRNA by metabolic propargyl labeling and sequencing," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    5. You Wu & Wenna Shao & Mengxiao Yan & Yuqin Wang & Pengfei Xu & Guoqiang Huang & Xiaofei Li & Brian D. Gregory & Jun Yang & Hongxia Wang & Xiang Yu, 2024. "Transfer learning enables identification of multiple types of RNA modifications using nanopore direct RNA sequencing," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    6. Hongna Zuo & Aiwei Wu & Mingwei Wang & Liquan Hong & Hu Wang, 2024. "tRNA m1A modification regulate HSC maintenance and self-renewal via mTORC1 signaling," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    7. Yanying Wang & Jing Wang & Xiaoyu Li & Xushen Xiong & Jianyi Wang & Ziheng Zhou & Xiaoxiao Zhu & Yang Gu & Dan Dominissini & Lei He & Yong Tian & Chengqi Yi & Zusen Fan, 2021. "N1-methyladenosine methylation in tRNA drives liver tumourigenesis by regulating cholesterol metabolism," Nature Communications, Nature, vol. 12(1), pages 1-19, December.

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