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Dynamic RNA acetylation revealed by quantitative cross-evolutionary mapping

Author

Listed:
  • Aldema Sas-Chen

    (Weizmann Institute of Science)

  • Justin M. Thomas

    (National Institutes of Health)

  • Donna Matzov

    (Weizmann Institute of Science)

  • Masato Taoka

    (Tokyo Metropolitan University)

  • Kellie D. Nance

    (National Institutes of Health)

  • Ronit Nir

    (Weizmann Institute of Science)

  • Keri M. Bryson

    (National Institutes of Health)

  • Ran Shachar

    (Weizmann Institute of Science)

  • Geraldy L. S. Liman

    (Colorado State University)

  • Brett W. Burkhart

    (Colorado State University)

  • Supuni Thalalla Gamage

    (National Institutes of Health)

  • Yuko Nobe

    (Tokyo Metropolitan University)

  • Chloe A. Briney

    (National Institutes of Health)

  • Michaella J. Levy

    (Stowers Institute for Medical Research)

  • Ryan T. Fuchs

    (New England Biolabs, Inc)

  • G. Brett Robb

    (New England Biolabs, Inc)

  • Jesse Hartmann

    (Weizmann Institute of Science)

  • Sunny Sharma

    (Rutgers University)

  • Qishan Lin

    (University at Albany)

  • Laurence Florens

    (Stowers Institute for Medical Research)

  • Michael P. Washburn

    (Stowers Institute for Medical Research)

  • Toshiaki Isobe

    (Tokyo Metropolitan University)

  • Thomas J. Santangelo

    (Colorado State University)

  • Moran Shalev-Benami

    (Weizmann Institute of Science)

  • Jordan L. Meier

    (National Institutes of Health)

  • Schraga Schwartz

    (Weizmann Institute of Science)

Abstract

N4-acetylcytidine (ac4C) is an ancient and highly conserved RNA modification that is present on tRNA and rRNA and has recently been investigated in eukaryotic mRNA1–3. However, the distribution, dynamics and functions of cytidine acetylation have yet to be fully elucidated. Here we report ac4C-seq, a chemical genomic method for the transcriptome-wide quantitative mapping of ac4C at single-nucleotide resolution. In human and yeast mRNAs, ac4C sites are not detected but can be induced—at a conserved sequence motif—via the ectopic overexpression of eukaryotic acetyltransferase complexes. By contrast, cross-evolutionary profiling revealed unprecedented levels of ac4C across hundreds of residues in rRNA, tRNA, non-coding RNA and mRNA from hyperthermophilic archaea. Ac4C is markedly induced in response to increases in temperature, and acetyltransferase-deficient archaeal strains exhibit temperature-dependent growth defects. Visualization of wild-type and acetyltransferase-deficient archaeal ribosomes by cryo-electron microscopy provided structural insights into the temperature-dependent distribution of ac4C and its potential thermoadaptive role. Our studies quantitatively define the ac4C landscape, providing a technical and conceptual foundation for elucidating the role of this modification in biology and disease4–6.

Suggested Citation

  • Aldema Sas-Chen & Justin M. Thomas & Donna Matzov & Masato Taoka & Kellie D. Nance & Ronit Nir & Keri M. Bryson & Ran Shachar & Geraldy L. S. Liman & Brett W. Burkhart & Supuni Thalalla Gamage & Yuko , 2020. "Dynamic RNA acetylation revealed by quantitative cross-evolutionary mapping," Nature, Nature, vol. 583(7817), pages 638-643, July.
    • Handle: RePEc:nat:nature:v:583:y:2020:i:7817:d:10.1038_s41586-020-2418-2
    DOI: 10.1038/s41586-020-2418-2
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    Citations

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    Cited by:

    1. K. Shanmugha Rajan & Hava Madmoni & Anat Bashan & Masato Taoka & Saurav Aryal & Yuko Nobe & Tirza Doniger & Beathrice Galili Kostin & Amit Blumberg & Smadar Cohen-Chalamish & Schraga Schwartz & Andre , 2023. "A single pseudouridine on rRNA regulates ribosome structure and function in the mammalian parasite Trypanosoma brucei," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    2. Jianheng Liu & Tao Huang & Wanying Chen & Chenhui Ding & Tianxuan Zhao & Xueni Zhao & Bing Cai & Yusen Zhang & Song Li & Ling Zhang & Maoguang Xue & Xiuju He & Wanzhong Ge & Canquan Zhou & Yanwen Xu &, 2022. "Developmental mRNA m5C landscape and regulatory innovations of massive m5C modification of maternal mRNAs in animals," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    3. Xue Jiang & Yu Cheng & Yuzhang Zhu & Caoling Xu & Qiaodan Li & Xuemei Xing & Wenqing Li & Jiaqi Zou & Lan Meng & Muhammad Azhar & Yuzhu Cao & Xianhong Tong & Weibing Qin & Xiaoli Zhu & Jianqiang Bao, 2023. "Maternal NAT10 orchestrates oocyte meiotic cell-cycle progression and maturation in mice," Nature Communications, Nature, vol. 14(1), pages 1-23, December.
    4. Belinda Baquero-Pérez & Ivaylo D. Yonchev & Anna Delgado-Tejedor & Rebeca Medina & Mireia Puig-Torrents & Ian Sudbery & Oguzhan Begik & Stuart A. Wilson & Eva Maria Novoa & Juana Díez, 2024. "N6-methyladenosine modification is not a general trait of viral RNA genomes," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    5. Nozomi Takahashi & Federica Franciosi & Enrico Maria Daldello & Xuan G. Luong & Peter Althoff & Xiaotian Wang & Marco Conti, 2023. "CPEB1-dependent disruption of the mRNA translation program in oocytes during maternal aging," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    6. Qin Yan & Jing Zhou & Ziyu Wang & Xiangya Ding & Xinyue Ma & Wan Li & Xuemei Jia & Shou-Jiang Gao & Chun Lu, 2023. "NAT10-dependent N4‐acetylcytidine modification mediates PAN RNA stability, KSHV reactivation, and IFI16-related inflammasome activation," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    7. Kristin A. Fluke & Ryan T. Fuchs & Yueh-Lin Tsai & Victoria Talbott & Liam Elkins & Hallie P. Febvre & Nan Dai & Eric J. Wolf & Brett W. Burkhart & Jackson Schiltz & G. Brett Robb & Ivan R. Corrêa & T, 2024. "The extensive m5C epitranscriptome of Thermococcus kodakarensis is generated by a suite of RNA methyltransferases that support thermophily," Nature Communications, Nature, vol. 15(1), pages 1-20, December.

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