IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-43194-2.html
   My bibliography  Save this article

Profiling stress-triggered RNA condensation with photocatalytic proximity labeling

Author

Listed:
  • Ziqi Ren

    (Peking University)

  • Wei Tang

    (Peking University)

  • Luxin Peng

    (Peking University)

  • Peng Zou

    (Peking University
    Peking University
    Chinese Institute for Brain Research (CIBR))

Abstract

Stress granules (SGs) are highly dynamic cytoplasmic membrane-less organelles that assemble when cells are challenged by stress. RNA molecules are sorted into SGs where they play important roles in maintaining the structural stability of SGs and regulating gene expression. Herein, we apply a proximity-dependent RNA labeling method, CAP-seq, to comprehensively investigate the content of SG-proximal transcriptome in live mammalian cells. CAP-seq captures 457 and 822 RNAs in arsenite- and sorbitol-induced SGs in HEK293T cells, respectively, revealing that SG enrichment is positively correlated with RNA length and AU content, but negatively correlated with translation efficiency. The high spatial specificity of CAP-seq dataset is validated by single-molecule FISH imaging. We further apply CAP-seq to map dynamic changes in SG-proximal transcriptome along the time course of granule assembly and disassembly processes. Our data portray a model of AU-rich and translationally repressed SG nanostructure that are memorized long after the removal of stress.

Suggested Citation

  • Ziqi Ren & Wei Tang & Luxin Peng & Peng Zou, 2023. "Profiling stress-triggered RNA condensation with photocatalytic proximity labeling," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43194-2
    DOI: 10.1038/s41467-023-43194-2
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-43194-2
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-43194-2?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. Fu Zheng & Chenxin Yu & Xinyue Zhou & Peng Zou, 2023. "Publisher Correction: Genetically encoded photocatalytic protein labeling enables spatially-resolved profiling of intracellular proteome," Nature Communications, Nature, vol. 14(1), pages 1-1, December.
    2. Yansheng Zhai & Xiaoyan Huang & Keren Zhang & Yuchen Huang & Yanlong Jiang & Jingwei Cui & Zhe Zhang & Cookson K. C. Chiu & Weiye Zhong & Gang Li, 2022. "Spatiotemporal-resolved protein networks profiling with photoactivation dependent proximity labeling," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    3. 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.
    4. Ryan J. Ries & Sara Zaccara & Pierre Klein & Anthony Olarerin-George & Sim Namkoong & Brian F. Pickering & Deepak P. Patil & Hojoong Kwak & Jun Hee Lee & Samie R. Jaffrey, 2019. "m6A enhances the phase separation potential of mRNA," Nature, Nature, vol. 571(7765), pages 424-428, July.
    5. Fu Zheng & Chenxin Yu & Xinyue Zhou & Peng Zou, 2023. "Genetically encoded photocatalytic protein labeling enables spatially-resolved profiling of intracellular proteome," Nature Communications, Nature, vol. 14(1), pages 1-14, 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. Ying Zhu & Kerem Can Akkaya & Julia Ruta & Nanako Yokoyama & Cong Wang & Max Ruwolt & Diogo Borges Lima & Martin Lehmann & Fan Liu, 2024. "Cross-link assisted spatial proteomics to map sub-organelle proteomes and membrane protein topologies," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    2. Dongmei Wang & Tao Sun & Yuan Xia & Zhe Zhao & Xue Sheng & Shuying Li & Yuechan Ma & Mingying Li & Xiuhua Su & Fan Zhang & Peng Li & Daoxin Ma & Jingjing Ye & Fei Lu & Chunyan Ji, 2023. "Homodimer-mediated phosphorylation of C/EBPα-p42 S16 modulates acute myeloid leukaemia differentiation through liquid-liquid phase separation," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    3. 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.
    4. 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.
    5. 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.
    6. 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.
    7. 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.
    8. 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.
    9. 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.
    10. 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.
    11. 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.
    12. Florian Pernin & Qiao-Ling Cui & Abdulshakour Mohammadnia & Milton G. F. Fernandes & Jeffery A. Hall & Myriam Srour & Roy W. R. Dudley & Stephanie E. J. Zandee & Wendy Klement & Alexandre Prat & Hanna, 2024. "Regulation of stress granule formation in human oligodendrocytes," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    13. Chen Wang & Hideki Tanizawa & Connor Hill & Aaron Havas & Qiang Zhang & Liping Liao & Xue Hao & Xue Lei & Lu Wang & Hao Nie & Yuan Qi & Bin Tian & Alessandro Gardini & Andrew V. Kossenkov & Aaron Gold, 2024. "METTL3-mediated chromatin contacts promote stress granule phase separation through metabolic reprogramming during senescence," Nature Communications, Nature, vol. 15(1), pages 1-16, 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:14:y:2023:i:1:d:10.1038_s41467-023-43194-2. 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.