IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-44987-9.html
   My bibliography  Save this article

Nuclear and cytoplasmic specific RNA binding proteome enrichment and its changes upon ferroptosis induction

Author

Listed:
  • Haofan Sun

    (Beijing Institute of Lifeomics)

  • Bin Fu

    (Beijing Institute of Lifeomics)

  • Xiaohong Qian

    (Beijing Institute of Lifeomics)

  • Ping Xu

    (Beijing Institute of Lifeomics)

  • Weijie Qin

    (Beijing Institute of Lifeomics
    Hebei University)

Abstract

The key role of RNA-binding proteins (RBPs) in posttranscriptional regulation of gene expression is intimately tied to their subcellular localization. Here, we show a subcellular-specific RNA labeling method for efficient enrichment and deep profiling of nuclear and cytoplasmic RBPs. A total of 1221 nuclear RBPs and 1333 cytoplasmic RBPs were enriched and identified using nuclear/cytoplasm targeting enrichment probes, representing an increase of 54.4% and 85.7% compared with previous reports. The probes were further applied in the omics-level investigation of subcellular-specific RBP-RNA interactions upon ferroptosis induction. Interestingly, large-scale RBPs display enhanced interaction with RNAs in nucleus but reduced association with RNAs in cytoplasm during ferroptosis process. Furthermore, we discovered dozens of nucleoplasmic translocation candidate RBPs upon ferroptosis induction and validated representative ones by immunofluorescence imaging. The enrichment of Tricarboxylic acid cycle in the translocation candidate RBPs may provide insights for investigating their possible roles in ferroptosis induced metabolism dysregulation.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-44987-9
    DOI: 10.1038/s41467-024-44987-9
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-44987-9
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-44987-9?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. Alessandra Zappulo & David Bruck & Camilla Ciolli Mattioli & Vedran Franke & Koshi Imami & Erik McShane & Mireia Moreno-Estelles & Lorenzo Calviello & Andrei Filipchyk & Esteban Peguero-Sanchez & Thom, 2017. "RNA localization is a key determinant of neurite-enriched proteome," Nature Communications, Nature, vol. 8(1), pages 1-13, December.
    2. Makoto Fukuda & Shiro Asano & Takahiro Nakamura & Makoto Adachi & Minoru Yoshida & Mitsuhiro Yanagida & Eisuke Nishida, 1997. "CRM1 is responsible for intracellular transport mediated by the nuclear export signal," Nature, Nature, vol. 390(6657), pages 308-311, November.
    3. 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.
    4. Eric L. Nostrand & Peter Freese & Gabriel A. Pratt & Xiaofeng Wang & Xintao Wei & Rui Xiao & Steven M. Blue & Jia-Yu Chen & Neal A. L. Cody & Daniel Dominguez & Sara Olson & Balaji Sundararaman & Liju, 2020. "A large-scale binding and functional map of human RNA-binding proteins," Nature, Nature, vol. 583(7818), pages 711-719, July.
    5. 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.
    6. Wei Qin & Samuel A. Myers & Dominique K. Carey & Steven A. Carr & Alice Y. Ting, 2021. "Spatiotemporally-resolved mapping of RNA binding proteins via functional proximity labeling reveals a mitochondrial mRNA anchor promoting stress recovery," Nature Communications, Nature, vol. 12(1), pages 1-19, December.
    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. 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.
    2. 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.
    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. 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.
    5. Matvei Khoroshkin & Andrey Buyan & Martin Dodel & Albertas Navickas & Johnny Yu & Fathima Trejo & Anthony Doty & Rithvik Baratam & Shaopu Zhou & Sean B. Lee & Tanvi Joshi & Kristle Garcia & Benedict C, 2024. "Systematic identification of post-transcriptional regulatory modules," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    6. 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.
    7. Timofey A. Karginov & Antoine Ménoret & Anthony T. Vella, 2022. "Optimal CD8+ T cell effector function requires costimulation-induced RNA-binding proteins that reprogram the transcript isoform landscape," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    8. Anna Knörlein & Chris P. Sarnowski & Tebbe Vries & Moritz Stoltz & Michael Götze & Ruedi Aebersold & Frédéric H.-T. Allain & Alexander Leitner & Jonathan Hall, 2022. "Nucleotide-amino acid π-stacking interactions initiate photo cross-linking in RNA-protein complexes," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    9. 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.
    10. Miquel Anglada-Girotto & Ludovica Ciampi & Sophie Bonnal & Sarah A. Head & Samuel Miravet-Verde & Luis Serrano, 2024. "In silico RNA isoform screening to identify potential cancer driver exons with therapeutic applications," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    11. Sarah E. Harris & Maria S. Alexis & Gilbert Giri & Francisco F. Cavazos & Yue Hu & Jernej Murn & Maria M. Aleman & Christopher B. Burge & Daniel Dominguez, 2024. "Understanding species-specific and conserved RNA-protein interactions in vivo and in vitro," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    12. Tamar Sapir & Aditya Kshirsagar & Anna Gorelik & Tsviya Olender & Ziv Porat & Ingrid E. Scheffer & David B. Goldstein & Orrin Devinsky & Orly Reiner, 2022. "Heterogeneous nuclear ribonucleoprotein U (HNRNPU) safeguards the developing mouse cortex," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    13. Erika Schaudy & Kathrin Hölz & Jory Lietard & Mark M. Somoza, 2022. "Simple synthesis of massively parallel RNA microarrays via enzymatic conversion from DNA microarrays," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    14. Mariela Cortés-López & Laura Schulz & Mihaela Enculescu & Claudia Paret & Bea Spiekermann & Mathieu Quesnel-Vallières & Manuel Torres-Diz & Sebastian Unic & Anke Busch & Anna Orekhova & Monika Kuban &, 2022. "High-throughput mutagenesis identifies mutations and RNA-binding proteins controlling CD19 splicing and CART-19 therapy resistance," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    15. Zili Song & Shuang Zhou & Hongjiao Zhang & Nancy P. Keller & Berl R. Oakley & Xiao Liu & Wen-Bing Yin, 2023. "Fungal secondary metabolism is governed by an RNA-binding protein CsdA/RsdA complex," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    16. Wei Hu & Yangjun Wu & Qili Shi & Jingni Wu & Deping Kong & Xiaohua Wu & Xianghuo He & Teng Liu & Shengli Li, 2022. "Systematic characterization of cancer transcriptome at transcript resolution," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    17. Xiangbin Ruan & Kaining Hu & Xiaochang Zhang, 2023. "PIE-seq: identifying RNA-binding protein targets by dual RNA-deaminase editing and sequencing," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    18. David Wang & Mathieu Quesnel-Vallieres & San Jewell & Moein Elzubeir & Kristen Lynch & Andrei Thomas-Tikhonenko & Yoseph Barash, 2023. "A Bayesian model for unsupervised detection of RNA splicing based subtypes in cancers," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    19. Haoran Zhu & Yuning Yang & Yunhe Wang & Fuzhou Wang & Yujian Huang & Yi Chang & Ka-chun Wong & Xiangtao Li, 2023. "Dynamic characterization and interpretation for protein-RNA interactions across diverse cellular conditions using HDRNet," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    20. Scott D. Findlay & Lindsay Romo & Christopher B. Burge, 2024. "Quantifying negative selection in human 3ʹ UTRs uncovers constrained targets of RNA-binding proteins," Nature Communications, Nature, vol. 15(1), pages 1-15, 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_s41467-024-44987-9. 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.