IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-37494-w.html
   My bibliography  Save this article

The RNA-binding protein landscapes differ between mammalian organs and cultured cells

Author

Listed:
  • Joel I. Perez-Perri

    (European Molecular Biology Laboratory)

  • Dunja Ferring-Appel

    (European Molecular Biology Laboratory)

  • Ina Huppertz

    (European Molecular Biology Laboratory
    Max Planck Institute for Biology of Ageing)

  • Thomas Schwarzl

    (European Molecular Biology Laboratory)

  • Sudeep Sahadevan

    (European Molecular Biology Laboratory)

  • Frank Stein

    (European Molecular Biology Laboratory)

  • Mandy Rettel

    (European Molecular Biology Laboratory)

  • Bruno Galy

    (Division of Virus-associated Carcinogenesis)

  • Matthias W. Hentze

    (European Molecular Biology Laboratory)

Abstract

System-wide approaches have unveiled an unexpected breadth of the RNA-bound proteomes of cultured cells. Corresponding information regarding RNA-binding proteins (RBPs) of mammalian organs is still missing, largely due to technical challenges. Here, we describe ex vivo enhanced RNA interactome capture (eRIC) to characterize the RNA-bound proteomes of three different mouse organs. The resulting organ atlases encompass more than 1300 RBPs active in brain, kidney or liver. Nearly a quarter (291) of these had formerly not been identified in cultured cells, with more than 100 being metabolic enzymes. Remarkably, RBP activity differs between organs independent of RBP abundance, suggesting organ-specific levels of control. Similarly, we identify systematic differences in RNA binding between animal organs and cultured cells. The pervasive RNA binding of enzymes of intermediary metabolism in organs points to tightly knit connections between gene expression and metabolism, and displays a particular enrichment for enzymes that use nucleotide cofactors. We describe a generically applicable refinement of the eRIC technology and provide an instructive resource of RBPs active in intact mammalian organs, including the brain.

Suggested Citation

  • Joel I. Perez-Perri & Dunja Ferring-Appel & Ina Huppertz & Thomas Schwarzl & Sudeep Sahadevan & Frank Stein & Mandy Rettel & Bruno Galy & Matthias W. Hentze, 2023. "The RNA-binding protein landscapes differ between mammalian organs and cultured cells," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37494-w
    DOI: 10.1038/s41467-023-37494-w
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-37494-w
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-37494-w?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. Feng Zhou & Yu Lu & Scott B. Ficarro & Guillaume Adelmant & Wenyu Jiang & C. John Luckey & Jarrod A. Marto, 2013. "Genome-scale proteome quantification by DEEP SEQ mass spectrometry," Nature Communications, Nature, vol. 4(1), pages 1-11, October.
    2. Cedric Ginestet, 2011. "ggplot2: Elegant Graphics for Data Analysis," Journal of the Royal Statistical Society Series A, Royal Statistical Society, vol. 174(1), pages 245-246, January.
    3. Jichun Zhou & Lihua Yang & Tianyu Zhong & Martin Mueller & Yi Men & Na Zhang & Juanke Xie & Karolyn Giang & Hunter Chung & Xueguang Sun & Lingeng Lu & Gordon G Carmichael & Hugh S Taylor & Yingqun Hua, 2015. "H19 lncRNA alters DNA methylation genome wide by regulating S-adenosylhomocysteine hydrolase," Nature Communications, Nature, vol. 6(1), pages 1-13, December.
    4. Benedikt M. Beckmann & Rastislav Horos & Bernd Fischer & Alfredo Castello & Katrin Eichelbaum & Anne-Marie Alleaume & Thomas Schwarzl & Tomaž Curk & Sophia Foehr & Wolfgang Huber & Jeroen Krijgsveld &, 2015. "The RNA-binding proteomes from yeast to man harbour conserved enigmRBPs," Nature Communications, Nature, vol. 6(1), pages 1-9, December.
    5. Chunqing Wang & Yongmei Li & Shuai Yan & Hao Wang & Xianfeng Shao & Mingming Xiao & Baicai Yang & Guoxuan Qin & Ruirui Kong & Ruibing Chen & Ning Zhang, 2020. "Interactome analysis reveals that lncRNA HULC promotes aerobic glycolysis through LDHA and PKM2," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    6. Thomas Conrad & Anne-Susann Albrecht & Veronica Rodrigues de Melo Costa & Sascha Sauer & David Meierhofer & Ulf Andersson Ørom, 2016. "Serial interactome capture of the human cell nucleus," Nature Communications, Nature, vol. 7(1), pages 1-11, September.
    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. Haofan Sun & Bin Fu & Xiaohong Qian & Ping Xu & Weijie Qin, 2024. "Nuclear and cytoplasmic specific RNA binding proteome enrichment and its changes upon ferroptosis induction," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    2. Andrew J. Heindel & Jeffrey W. Brulet & Xiantao Wang & Michael W. Founds & Adam H. Libby & Dina L. Bai & Michael C. Lemke & David M. Leace & Thurl E. Harris & Markus Hafner & Ku-Lung Hsu, 2023. "Chemoproteomic capture of RNA binding activity in living cells," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    3. Johanna Luige & Alexandros Armaos & Gian Gaetano Tartaglia & Ulf Andersson Vang Ørom, 2024. "Predicting nuclear G-quadruplex RNA-binding proteins with roles in transcription and phase separation," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    4. Qingtai Su & Aurélie Bouteau & Jacob Cardenas & Balaji Uthra & Yuanyaun Wang & Cynthia Smitherman & Jinghua Gu & Botond Z Igyártó, 2020. "Brief communication: Long-term absence of Langerhans cells alters the gene expression profile of keratinocytes and dendritic epidermal T cells," PLOS ONE, Public Library of Science, vol. 15(1), pages 1-9, January.
    5. Liang-Cui Chu & Pedro Arede & Wei Li & Erika C. Urdaneta & Ivayla Ivanova & Stuart W. McKellar & Jimi C. Wills & Theresa Fröhlich & Alexander Kriegsheim & Benedikt M. Beckmann & Sander Granneman, 2022. "The RNA-bound proteome of MRSA reveals post-transcriptional roles for helix-turn-helix DNA-binding and Rossmann-fold proteins," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    6. Tom G. Richardson & Daniel J. M. Crouch & Grace M. Power & Fernanda Morales-Berstein & Emma Hazelwood & Si Fang & Yoonsu Cho & Jamie R. J. Inshaw & Catherine C. Robertson & Carlo Sidore & Francesco Cu, 2022. "Childhood body size directly increases type 1 diabetes risk based on a lifecourse Mendelian randomization approach," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    7. Oksana V. Stanevich & Evgeniia I. Alekseeva & Maria Sergeeva & Artem V. Fadeev & Kseniya S. Komissarova & Anna A. Ivanova & Tamara S. Simakova & Kirill A. Vasilyev & Anna-Polina Shurygina & Marina A. , 2023. "SARS-CoV-2 escape from cytotoxic T cells during long-term COVID-19," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    8. Lingqian Xu & Debapriya Mondal & David A. Polya, 2020. "Positive Association of Cardiovascular Disease (CVD) with Chronic Exposure to Drinking Water Arsenic (As) at Concentrations below the WHO Provisional Guideline Value: A Systematic Review and Meta-anal," IJERPH, MDPI, vol. 17(7), pages 1-24, April.
    9. Ebru Aydin & Silke Schreiner & Jacqueline Böhme & Birte Keil & Jan Weber & Bojan Žunar & Timo Glatter & Cornelia Kilchert, 2024. "DEAD-box ATPase Dbp2 is the key enzyme in an mRNP assembly checkpoint at the 3’-end of genes and involved in the recycling of cleavage factors," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    10. Xueman Chen & Rong Luo & Yunmei Zhang & Shuying Ye & Xin Zeng & Jiang Liu & Di Huang & Yujie Liu & Qiang Liu & Man-Li Luo & Erwei Song, 2022. "Long noncoding RNA DIO3OS induces glycolytic-dominant metabolic reprogramming to promote aromatase inhibitor resistance in breast cancer," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    11. Yan Ting Shue & Alexandros P. Drainas & Nancy Yanzhe Li & Sarah M. Pearsall & Derrick Morgan & Nasa Sinnott-Armstrong & Susan Q. Hipkins & Garry L. Coles & Jing Shan Lim & Anthony E. Oro & Kathryn L. , 2022. "A conserved YAP/Notch/REST network controls the neuroendocrine cell fate in the lungs," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    12. Junliang Yin & Xiaowen Han & Yongxing Zhu & Zhengwu Fang & Derong Gao & Dongfang Ma, 2022. "Transcriptome Profiles of Circular RNAs in Common Wheat during Fusarium Head Blight Disease," Data, MDPI, vol. 7(9), pages 1-8, August.
    13. Kei Hiruma & Seishiro Aoki & Junya Takino & Takeshi Higa & Yuniar Devi Utami & Akito Shiina & Masanori Okamoto & Masami Nakamura & Nanami Kawamura & Yoshihiro Ohmori & Ryohei Sugita & Keitaro Tanoi & , 2023. "A fungal sesquiterpene biosynthesis gene cluster critical for mutualist-pathogen transition in Colletotrichum tofieldiae," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    14. Lukas Bartonek & Bojan Zagrovic, 2017. "mRNA/protein sequence complementarity and its determinants: The impact of affinity scales," PLOS Computational Biology, Public Library of Science, vol. 13(7), pages 1-16, July.
    15. Gabriela Montejo-Kovacevich & Joana I. Meier & Caroline N. Bacquet & Ian A. Warren & Yingguang Frank Chan & Marek Kucka & Camilo Salazar & Nicol Rueda-M & Stephen H. Montgomery & W. Owen McMillan & Kr, 2022. "Repeated genetic adaptation to altitude in two tropical butterflies," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    16. Meeli Mullari & Nicolas Fossat & Niels H. Skotte & Andrea Asenjo-Martinez & David T. Humphreys & Jens Bukh & Agnete Kirkeby & Troels K. H. Scheel & Michael L. Nielsen, 2023. "Characterising the RNA-binding protein atlas of the mammalian brain uncovers RBM5 misregulation in mouse models of Huntington’s disease," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    17. Gerard Llimos & Vincent Gardeux & Ute Koch & Judith F. Kribelbauer & Antonina Hafner & Daniel Alpern & Joern Pezoldt & Maria Litovchenko & Julie Russeil & Riccardo Dainese & Riccardo Moia & Abdurraouf, 2022. "A leukemia-protective germline variant mediates chromatin module formation via transcription factor nucleation," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    18. Alastair G. Kerr & Zuoneng Wang & Na Wang & Kelvin H. M. Kwok & Jutta Jalkanen & Alison Ludzki & Simon Lecoutre & Dominique Langin & Martin O. Bergo & Ingrid Dahlman & Carsten Mim & Peter Arner & Hui , 2022. "The long noncoding RNA ADIPINT regulates human adipocyte metabolism via pyruvate carboxylase," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    19. JohnCarlo Kristofich & Christopher V. Nicchitta, 2023. "Signal-noise metrics for RNA binding protein identification reveal broad spectrum protein-RNA interaction frequencies and dynamics," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    20. Maxwell P. Gold & Winnie Ong & Andrew M. Masteller & David R. Ghasemi & Julie Anne Galindo & Noel R. Park & Nhan C. Huynh & Aneesh Donde & Veronika Pister & Raul A. Saurez & Maria C. Vladoiu & Grace H, 2024. "Developmental basis of SHH medulloblastoma heterogeneity," Nature Communications, Nature, vol. 15(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:14:y:2023:i:1:d:10.1038_s41467-023-37494-w. 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.