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Decoding the genomic landscape of chromatin-associated biomolecular condensates

Author

Listed:
  • Zhaowei Yu

    (Tongji University)

  • Qi Wang

    (Tongji University)

  • Qichen Zhang

    (Naval Medical University
    Lingang Laboratory)

  • Yawen Tian

    (Lingang Laboratory)

  • Guo Yan

    (Lingang Laboratory)

  • Jidong Zhu

    (Etern Biopharma)

  • Guangya Zhu

    (Lingang Laboratory)

  • Yong Zhang

    (Tongji University)

Abstract

Biomolecular condensates play a significant role in chromatin activities, primarily by concentrating and compartmentalizing proteins and/or nucleic acids. However, their genomic landscapes and compositions remain largely unexplored due to a lack of dedicated computational tools for systematic identification in vivo. To address this, we develop CondSigDetector, a computational framework designed to detect condensate-like chromatin-associated protein co-occupancy signatures (CondSigs), to predict genomic loci and component proteins of distinct chromatin-associated biomolecular condensates. Applying this framework to mouse embryonic stem cells (mESC) and human K562 cells enable us to depict the high-resolution genomic landscape of chromatin-associated biomolecular condensates, and uncover both known and potentially unknown biomolecular condensates. Multi-omics analysis and experimental validation further verify the condensation properties of CondSigs. Additionally, our investigation sheds light on the impact of chromatin-associated biomolecular condensates on chromatin activities. Collectively, CondSigDetector provides an approach to decode the genomic landscape of chromatin-associated condensates, facilitating a deeper understanding of their biological functions and underlying mechanisms in cells.

Suggested Citation

  • Zhaowei Yu & Qi Wang & Qichen Zhang & Yawen Tian & Guo Yan & Jidong Zhu & Guangya Zhu & Yong Zhang, 2024. "Decoding the genomic landscape of chromatin-associated biomolecular condensates," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51426-2
    DOI: 10.1038/s41467-024-51426-2
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    1. Bin Duan & Chi Zhou & Chengyu Zhu & Yifei Yu & Gaoyang Li & Shihua Zhang & Chao Zhang & Xiangyun Ye & Hanhui Ma & Shen Qu & Zhiyuan Zhang & Ping Wang & Shuyang Sun & Qi Liu, 2019. "Model-based understanding of single-cell CRISPR screening," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    2. Raphaël Margueron & Danny Reinberg, 2011. "The Polycomb complex PRC2 and its mark in life," Nature, Nature, vol. 469(7330), pages 343-349, January.
    3. Jeong Hyun Ahn & Eric S. Davis & Timothy A. Daugird & Shuai Zhao & Ivana Yoseli Quiroga & Hidetaka Uryu & Jie Li & Aaron J. Storey & Yi-Hsuan Tsai & Daniel P. Keeley & Samuel G. Mackintosh & Ricky D. , 2021. "Phase separation drives aberrant chromatin looping and cancer development," Nature, Nature, vol. 595(7868), pages 591-595, July.
    4. Shuang Hou & Jiaojiao Hu & Zhaowei Yu & Dan Li & Cong Liu & Yong Zhang, 2024. "Machine learning predictor PSPire screens for phase-separating proteins lacking intrinsically disordered regions," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    5. Jesse R. Dixon & Siddarth Selvaraj & Feng Yue & Audrey Kim & Yan Li & Yin Shen & Ming Hu & Jun S. Liu & Bing Ren, 2012. "Topological domains in mammalian genomes identified by analysis of chromatin interactions," Nature, Nature, vol. 485(7398), pages 376-380, May.
    6. Matthias Altmeyer & Kai J. Neelsen & Federico Teloni & Irina Pozdnyakova & Stefania Pellegrino & Merete Grøfte & Maj-Britt Druedahl Rask & Werner Streicher & Stephanie Jungmichel & Michael Lund Nielse, 2015. "Liquid demixing of intrinsically disordered proteins is seeded by poly(ADP-ribose)," Nature Communications, Nature, vol. 6(1), pages 1-12, November.
    7. Junqi Kuang & Ziwei Zhai & Pengli Li & Ruona Shi & Wenjing Guo & Yuxiang Yao & Jing Guo & Guoqing Zhao & Jiangpin He & Shuyang Xu & Chuman Wu & Shengyong Yu & Chunhua Zhou & Linlin Wu & Yue Qin & Baom, 2021. "SS18 regulates pluripotent-somatic transition through phase separation," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    8. Amy R. Strom & Alexander V. Emelyanov & Mustafa Mir & Dmitry V. Fyodorov & Xavier Darzacq & Gary H. Karpen, 2017. "Phase separation drives heterochromatin domain formation," Nature, Nature, vol. 547(7662), pages 241-245, July.
    9. Maria Hondele & Ruchika Sachdev & Stephanie Heinrich & Juan Wang & Pascal Vallotton & Beatriz M. A. Fontoura & Karsten Weis, 2019. "DEAD-box ATPases are global regulators of phase-separated organelles," Nature, Nature, vol. 573(7772), pages 144-148, September.
    10. Yang Eric Guo & John C. Manteiga & Jonathan E. Henninger & Benjamin R. Sabari & Alessandra Dall’Agnese & Nancy M. Hannett & Jan-Hendrik Spille & Lena K. Afeyan & Alicia V. Zamudio & Krishna Shrinivas , 2019. "Pol II phosphorylation regulates a switch between transcriptional and splicing condensates," Nature, Nature, vol. 572(7770), pages 543-548, August.
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