IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-53973-0.html
   My bibliography  Save this article

Charting and probing the activity of ADARs in human development and cell-fate specification

Author

Listed:
  • Amir Dailamy

    (University of California San Diego)

  • Weiqi Lyu

    (University of California San Diego
    Altos Labs)

  • Sami Nourreddine

    (University of California San Diego)

  • Michael Tong

    (University of California San Diego)

  • Joseph Rainaldi

    (University of California San Diego
    University of California San Diego)

  • Daniella McDonald

    (University of California San Diego
    University of California San Diego)

  • Rebecca Panwala

    (University of California San Diego)

  • Alysson Muotri

    (University of California San Diego)

  • Michael S. Breen

    (Icahn School of Medicine at Mount Sinai)

  • Kun Zhang

    (University of California San Diego
    Altos Labs)

  • Prashant Mali

    (University of California San Diego)

Abstract

Adenosine deaminases acting on RNA (ADARs) impact diverse cellular processes and pathological conditions, but their functions in early cell-fate specification remain less understood. To gain insights here, we began by charting time-course RNA editing profiles in human organs from fetal to adult stages. Next, we utilized hPSC differentiation to experimentally probe ADARs, harnessing brain organoids as neural specific, and teratomas as pan-tissue developmental models. We show that time-series teratomas faithfully recapitulate fetal developmental trends, and motivated by this, conducted pan-tissue, single-cell CRISPR-KO screens of ADARs in teratomas. Knocking out ADAR leads to a global decrease in RNA editing across all germ-layers. Intriguingly, knocking out ADAR leads to an enrichment of adipogenic cells, revealing a role for ADAR in human adipogenesis. Collectively, we present a multi-pronged framework charting time-resolved RNA editing profiles and coupled ADAR perturbations in developmental models, thereby shedding light on the role of ADARs in cell-fate specification.

Suggested Citation

  • Amir Dailamy & Weiqi Lyu & Sami Nourreddine & Michael Tong & Joseph Rainaldi & Daniella McDonald & Rebecca Panwala & Alysson Muotri & Michael S. Breen & Kun Zhang & Prashant Mali, 2024. "Charting and probing the activity of ADARs in human development and cell-fate specification," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-53973-0
    DOI: 10.1038/s41467-024-53973-0
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-53973-0
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-53973-0?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. 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.
    2. Winston H. Cuddleston & Junhao Li & Xuanjia Fan & Alexey Kozenkov & Matthew Lalli & Shahrukh Khalique & Stella Dracheva & Eran A. Mukamel & Michael S. Breen, 2022. "Cellular and genetic drivers of RNA editing variation in the human brain," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    3. Katarzyna Niescierowicz & Leszek Pryszcz & Cristina Navarrete & Eugeniusz Tralle & Agata Sulej & Karim Abu Nahia & Marta Elżbieta Kasprzyk & Katarzyna Misztal & Abhishek Pateria & Adrianna Pakuła & Ma, 2022. "Adar-mediated A-to-I editing is required for embryonic patterning and innate immune response regulation in zebrafish," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    4. Matthew B. Buechler & Rachana N. Pradhan & Akshay T. Krishnamurty & Christian Cox & Aslihan Karabacak Calviello & Amber W. Wang & Yeqing Angela Yang & Lucinda Tam & Roger Caothien & Merone Roose-Girma, 2021. "Cross-tissue organization of the fibroblast lineage," Nature, Nature, vol. 593(7860), pages 575-579, May.
    5. Nicholas W. Hubbard & Joshua M. Ames & Megan Maurano & Lan H. Chu & Kim Y. Somfleth & Nandan S. Gokhale & Margo Werner & Jessica M. Snyder & Katrina Lichauco & Ram Savan & Daniel B. Stetson & Andrew O, 2022. "ADAR1 mutation causes ZBP1-dependent immunopathology," Nature, Nature, vol. 607(7920), pages 769-775, July.
    6. Qiao-qiao He & Yu Huang & Longyu Nie & Sheng Ren & Gang Xu & Feiyan Deng & Zhikui Cheng & Qi Zuo & Lin Zhang & Huanhuan Cai & Qiming Wang & Fubing Wang & Hong Ren & Huan Yan & Ke Xu & Li Zhou & Mengji, 2023. "MAVS integrates glucose metabolism and RIG-I-like receptor signaling," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    7. Hadas Tsivion-Visbord & Eli Kopel & Ariel Feiglin & Tamar Sofer & Ran Barzilay & Tali Ben-Zur & Orly Yaron & Daniel Offen & Erez Y. Levanon, 2020. "Increased RNA editing in maternal immune activation model of neurodevelopmental disease," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    8. 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.
    9. 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.
    Full references (including those not matched with items on IDEAS)

    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. 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.
    2. 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.
    3. 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.
    4. Kotaro Shimizu & Junichi Kikuta & Yumi Ohta & Yutaka Uchida & Yu Miyamoto & Akito Morimoto & Shinya Yari & Takashi Sato & Takefumi Kamakura & Kazuo Oshima & Ryusuke Imai & Yu-Chen Liu & Daisuke Okuzak, 2023. "Single-cell transcriptomics of human cholesteatoma identifies an activin A-producing osteoclastogenic fibroblast subset inducing bone destruction," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    5. LiangYu Zhao & Sha Han & HengChuan Su & JianYing Li & ErLei Zhi & Peng Li & ChenCheng Yao & RuHui Tian & HuiXing Chen & HuiRong Chen & JiaQiang Luo & ChenKun Shi & ZhiYong Ji & JianLin Hu & Gang Wu & , 2022. "Single-cell transcriptome atlas of the human corpus cavernosum," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    6. Karthika Devi Kiran Kumar & Shubhangi Singh & Stella Maria Schmelzle & Paul Vogel & Carolin Fruhner & Alfred Hanswillemenke & Adrian Brun & Jacqueline Wettengel & Yvonne Füll & Lukas Funk & Valentin M, 2024. "An improved SNAP-ADAR tool enables efficient RNA base editing to interfere with post-translational protein modification," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    7. Yiyi Ma & Eric B. Dammer & Daniel Felsky & Duc M. Duong & Hans-Ulrich Klein & Charles C. White & Maotian Zhou & Benjamin A. Logsdon & Cristin McCabe & Jishu Xu & Minghui Wang & Thomas S. Wingo & James, 2021. "Atlas of RNA editing events affecting protein expression in aged and Alzheimer’s disease human brain tissue," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    8. Fabian Peisker & Maurice Halder & James Nagai & Susanne Ziegler & Nadine Kaesler & Konrad Hoeft & Ronghui Li & Eric M. J. Bindels & Christoph Kuppe & Julia Moellmann & Michael Lehrke & Christian Stopp, 2022. "Mapping the cardiac vascular niche in heart failure," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    9. Shuo Wang & An Song & Jun Xie & Yuan-Yuan Wang & Wen-Da Wang & Meng-Jie Zhang & Zhi-Zhong Wu & Qi-Chao Yang & Hao Li & Junjie Zhang & Zhi-Jun Sun, 2024. "Fn-OMV potentiates ZBP1-mediated PANoptosis triggered by oncolytic HSV-1 to fuel antitumor immunity," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    10. Martin Uhrbom & Lars Muhl & Guillem Genové & Jianping Liu & Henrik Palmgren & Ida Alexandersson & Fredrik Karlsson & Alex-Xianghua Zhou & Sandra Lunnerdal & Sonja Gustafsson & Byambajav Buyandelger & , 2024. "Adipose stem cells are sexually dimorphic cells with dual roles as preadipocytes and resident fibroblasts," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    11. Lucas Massier & Jutta Jalkanen & Merve Elmastas & Jiawei Zhong & Tongtong Wang & Pamela A. Nono Nankam & Scott Frendo-Cumbo & Jesper Bäckdahl & Narmadha Subramanian & Takuya Sekine & Alastair G. Kerr , 2023. "An integrated single cell and spatial transcriptomic map of human white adipose tissue," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    12. Kathryn Weinand & Saori Sakaue & Aparna Nathan & Anna Helena Jonsson & Fan Zhang & Gerald F. M. Watts & Majd Al Suqri & Zhu Zhu & Deepak A. Rao & Jennifer H. Anolik & Michael B. Brenner & Laura T. Don, 2024. "The chromatin landscape of pathogenic transcriptional cell states in rheumatoid arthritis," Nature Communications, Nature, vol. 15(1), pages 1-25, December.
    13. Benjamin Padilla-Morales & Alin P. Acuña-Alonzo & Huseyin Kilili & Atahualpa Castillo-Morales & Karina Díaz-Barba & Kathryn H. Maher & Laurie Fabian & Evangelos Mourkas & Tamás Székely & Martin-Alejan, 2024. "Sexual size dimorphism in mammals is associated with changes in the size of gene families related to brain development," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    14. Julia M. Houthuijzen & Roebi Bruijn & Eline Burg & Anne Paulien Drenth & Ellen Wientjens & Tamara Filipovic & Esme Bullock & Chiara S. Brambillasca & Emilia M. Pulver & Marja Nieuwland & Iris Rink & F, 2023. "CD26-negative and CD26-positive tissue-resident fibroblasts contribute to functionally distinct CAF subpopulations in breast cancer," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    15. Miguel Angel Brieño-Enríquez & Mariela Faykoo-Martinez & Meagan Goben & Jennifer K. Grenier & Ashley McGrath & Alexandra M. Prado & Jacob Sinopoli & Kate Wagner & Patrick T. Walsh & Samia H. Lopa & Di, 2023. "Postnatal oogenesis leads to an exceptionally large ovarian reserve in naked mole-rats," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    16. Paula Punzon-Jimenez & Alba Machado-Lopez & Raul Perez-Moraga & Jaime Llera-Oyola & Daniela Grases & Marta Galvez-Viedma & Mustafa Sibai & Elena Satorres-Perez & Susana Lopez-Agullo & Rafael Badenes &, 2024. "Effect of aging on the human myometrium at single-cell resolution," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    17. Shunsuke Tanigawa & Etsuko Tanaka & Koichiro Miike & Tomoko Ohmori & Daisuke Inoue & Chen-Leng Cai & Atsuhiro Taguchi & Akio Kobayashi & Ryuichi Nishinakamura, 2022. "Generation of the organotypic kidney structure by integrating pluripotent stem cell-derived renal stroma," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    18. Christopher J. Hanley & Sara Waise & Matthew J. Ellis & Maria A. Lopez & Wai Y. Pun & Julian Taylor & Rachel Parker & Lucy M. Kimbley & Serena J. Chee & Emily C. Shaw & Jonathan West & Aiman Alzetani , 2023. "Single-cell analysis reveals prognostic fibroblast subpopulations linked to molecular and immunological subtypes of lung cancer," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    19. Caroline B. Albertin & Sofia Medina-Ruiz & Therese Mitros & Hannah Schmidbaur & Gustavo Sanchez & Z. Yan Wang & Jane Grimwood & Joshua J. C. Rosenthal & Clifton W. Ragsdale & Oleg Simakov & Daniel S. , 2022. "Genome and transcriptome mechanisms driving cephalopod evolution," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    20. Chen Ni & Xiaohan Lou & Xiaohan Yao & Linlin Wang & Jiajia Wan & Xixi Duan & Jialu Liang & Kaili Zhang & Yuanyuan Yang & Li Zhang & Chanjun Sun & Zhenzhen Li & Ming Wang & Linyu Zhu & Dekang Lv & Zhih, 2022. "ZIP1+ fibroblasts protect lung cancer against chemotherapy via connexin-43 mediated intercellular Zn2+ transfer," Nature Communications, Nature, vol. 13(1), pages 1-20, 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:15:y:2024:i:1:d:10.1038_s41467-024-53973-0. 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.