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Landscape of adenosine-to-inosine RNA recoding across human tissues

Author

Listed:
  • Orshay Gabay

    (Bar-Ilan University)

  • Yoav Shoshan

    (Tel Aviv University)

  • Eli Kopel

    (Bar-Ilan University)

  • Udi Ben-Zvi

    (Bar-Ilan University)

  • Tomer D. Mann

    (Tel Aviv University)

  • Noam Bressler

    (Tel Aviv University)

  • Roni Cohen‐Fultheim

    (Bar-Ilan University)

  • Amos A. Schaffer

    (Bar-Ilan University)

  • Shalom Hillel Roth

    (Bar-Ilan University)

  • Ziv Tzur

    (Bar-Ilan University)

  • Erez Y. Levanon

    (Bar-Ilan University
    Bar‐Ilan University)

  • Eli Eisenberg

    (Tel Aviv University)

Abstract

RNA editing by adenosine deaminases changes the information encoded in the mRNA from its genomic blueprint. Editing of protein-coding sequences can introduce novel, functionally distinct, protein isoforms and diversify the proteome. The functional importance of a few recoding sites has been appreciated for decades. However, systematic methods to uncover these sites perform poorly, and the full repertoire of recoding in human and other mammals is unknown. Here we present a new detection approach, and analyze 9125 GTEx RNA-seq samples, to produce a highly-accurate atlas of 1517 editing sites within the coding region and their editing levels across human tissues. Single-cell RNA-seq data shows protein recoding contributes to the variability across cell subpopulations. Most highly edited sites are evolutionary conserved in non-primate mammals, attesting for adaptation. This comprehensive set can facilitate understanding of the role of recoding in human physiology and diseases.

Suggested Citation

  • Orshay Gabay & Yoav Shoshan & Eli Kopel & Udi Ben-Zvi & Tomer D. Mann & Noam Bressler & Roni Cohen‐Fultheim & Amos A. Schaffer & Shalom Hillel Roth & Ziv Tzur & Erez Y. Levanon & Eli Eisenberg, 2022. "Landscape of adenosine-to-inosine RNA recoding across human tissues," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28841-4
    DOI: 10.1038/s41467-022-28841-4
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    as
    1. Kyle J. Travaglini & Ahmad N. Nabhan & Lolita Penland & Rahul Sinha & Astrid Gillich & Rene V. Sit & Stephen Chang & Stephanie D. Conley & Yasuo Mori & Jun Seita & Gerald J. Berry & Joseph B. Shrager , 2020. "A molecular cell atlas of the human lung from single-cell RNA sequencing," Nature, Nature, vol. 587(7835), pages 619-625, November.
    2. Haley J. Abel & David E. Larson & Allison A. Regier & Colby Chiang & Indraniel Das & Krishna L. Kanchi & Ryan M. Layer & Benjamin M. Neale & William J. Salerno & Catherine Reeves & Steven Buyske & Tar, 2020. "Mapping and characterization of structural variation in 17,795 human genomes," Nature, Nature, vol. 583(7814), pages 83-89, July.
    3. Feng Yue & Yong Cheng & Alessandra Breschi & Jeff Vierstra & Weisheng Wu & Tyrone Ryba & Richard Sandstrom & Zhihai Ma & Carrie Davis & Benjamin D. Pope & Yin Shen & Dmitri D. Pervouchine & Sarah Djeb, 2014. "A comparative encyclopedia of DNA elements in the mouse genome," Nature, Nature, vol. 515(7527), pages 355-364, November.
    4. Margarida Cardoso-Moreira & Jean Halbert & Delphine Valloton & Britta Velten & Chunyan Chen & Yi Shao & Angélica Liechti & Kelly Ascenção & Coralie Rummel & Svetlana Ovchinnikova & Pavel V. Mazin & Io, 2019. "Gene expression across mammalian organ development," Nature, Nature, vol. 571(7766), pages 505-509, July.
    5. Meng How Tan & Qin Li & Raghuvaran Shanmugam & Robert Piskol & Jennefer Kohler & Amy N. Young & Kaiwen Ivy Liu & Rui Zhang & Gokul Ramaswami & Kentaro Ariyoshi & Ankita Gupte & Liam P. Keegan & Cyril , 2017. "Dynamic landscape and regulation of RNA editing in mammals," Nature, Nature, vol. 550(7675), pages 249-254, October.
    6. Julie M. Eggington & Tom Greene & Brenda L. Bass, 2011. "Predicting sites of ADAR editing in double-stranded RNA," Nature Communications, Nature, vol. 2(1), pages 1-9, September.
    7. Ying Yu & James C. Fuscoe & Chen Zhao & Chao Guo & Meiwen Jia & Tao Qing & Desmond I. Bannon & Lee Lancashire & Wenjun Bao & Tingting Du & Heng Luo & Zhenqiang Su & Wendell D. Jones & Carrie L. Moland, 2014. "A rat RNA-Seq transcriptomic BodyMap across 11 organs and 4 developmental stages," Nature Communications, Nature, vol. 5(1), pages 1-11, May.
    8. Rebecca D. Hodge & Trygve E. Bakken & Jeremy A. Miller & Kimberly A. Smith & Eliza R. Barkan & Lucas T. Graybuck & Jennie L. Close & Brian Long & Nelson Johansen & Osnat Penn & Zizhen Yao & Jeroen Egg, 2019. "Conserved cell types with divergent features in human versus mouse cortex," Nature, Nature, vol. 573(7772), pages 61-68, September.
    9. Daohan Jiang & Jianzhi Zhang, 2019. "The preponderance of nonsynonymous A-to-I RNA editing in coleoids is nonadaptive," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
    10. Hagit T. Porath & Shai Carmi & Erez Y. Levanon, 2014. "A genome-wide map of hyper-edited RNA reveals numerous new sites," Nature Communications, Nature, vol. 5(1), pages 1-10, December.
    11. Shai Carmi & Ken Y. Hui & Ethan Kochav & Xinmin Liu & James Xue & Fillan Grady & Saurav Guha & Kinnari Upadhyay & Dan Ben-Avraham & Semanti Mukherjee & B. Monica Bowen & Tinu Thomas & Joseph Vijai & M, 2014. "Sequencing an Ashkenazi reference panel supports population-targeted personal genomics and illuminates Jewish and European origins," Nature Communications, Nature, vol. 5(1), pages 1-9, December.
    12. David Brawand & Magali Soumillon & Anamaria Necsulea & Philippe Julien & Gábor Csárdi & Patrick Harrigan & Manuela Weier & Angélica Liechti & Ayinuer Aximu-Petri & Martin Kircher & Frank W. Albert & U, 2011. "The evolution of gene expression levels in mammalian organs," Nature, Nature, vol. 478(7369), pages 343-348, October.
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    2. Marlon S. Zambrano-Mila & Monika Witzenberger & Zohar Rosenwasser & Anna Uzonyi & Ronit Nir & Shay Ben-Aroya & Erez Y. Levanon & Schraga Schwartz, 2023. "Dissecting the basis for differential substrate specificity of ADAR1 and ADAR2," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    3. Miguel Rodriguez de los Santos & Brian H. Kopell & Ariela Buxbaum Grice & Gauri Ganesh & Andy Yang & Pardis Amini & Lora E. Liharska & Eric Vornholt & John F. Fullard & Pengfei Dong & Eric Park & Sara, 2024. "Divergent landscapes of A-to-I editing in postmortem and living human brain," Nature Communications, Nature, vol. 15(1), pages 1-15, December.

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