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Global mapping of RNA-chromatin contacts reveals a proximity-dominated connectivity model for ncRNA-gene interactions

Author

Listed:
  • Charles Limouse

    (Stanford University, Stanford)

  • Owen K. Smith

    (Stanford University, Stanford)

  • David Jukam

    (Stanford University, Stanford)

  • Kelsey A. Fryer

    (Stanford University, Stanford
    Stanford University, Stanford)

  • William J. Greenleaf

    (Stanford University, Stanford)

  • Aaron F. Straight

    (Stanford University, Stanford)

Abstract

Non-coding RNAs (ncRNAs) are transcribed throughout the genome and provide regulatory inputs to gene expression through their interaction with chromatin. Yet, the genomic targets and functions of most ncRNAs are unknown. Here we use chromatin-associated RNA sequencing (ChAR-seq) to map the global network of ncRNA interactions with chromatin in human embryonic stem cells and the dynamic changes in interactions during differentiation into definitive endoderm. We uncover general principles governing the organization of the RNA-chromatin interactome, demonstrating that nearly all ncRNAs exclusively interact with genes in close three-dimensional proximity to their locus and provide a model predicting the interactome. We uncover RNAs that interact with many loci across the genome and unveil thousands of unannotated RNAs that dynamically interact with chromatin. By relating the dynamics of the interactome to changes in gene expression, we demonstrate that activation or repression of individual genes is unlikely to be controlled by a single ncRNA.

Suggested Citation

  • Charles Limouse & Owen K. Smith & David Jukam & Kelsey A. Fryer & William J. Greenleaf & Aaron F. Straight, 2023. "Global mapping of RNA-chromatin contacts reveals a proximity-dominated connectivity model for ncRNA-gene interactions," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41848-9
    DOI: 10.1038/s41467-023-41848-9
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    1. 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.
    2. Miguel Casanova & Madeleine Moscatelli & Louis Édouard Chauvière & Christophe Huret & Julia Samson & Tharvesh Moideen Liyakat Ali & Olga Rosspopoff & Claire Rougeulle, 2019. "A primate-specific retroviral enhancer wires the XACT lncRNA into the core pluripotency network in humans," Nature Communications, Nature, vol. 10(1), pages 1-14, December.
    3. Lovorka Stojic & Malwina Niemczyk & Arturo Orjalo & Yoko Ito & Anna Elisabeth Maria Ruijter & Santiago Uribe-Lewis & Nimesh Joseph & Stephen Weston & Suraj Menon & Duncan T. Odom & John Rinn & Fanni G, 2016. "Transcriptional silencing of long noncoding RNA GNG12-AS1 uncouples its transcriptional and product-related functions," Nature Communications, Nature, vol. 7(1), pages 1-14, April.
    4. 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.
    5. Tae-Kyung Kim & Martin Hemberg & Jesse M. Gray & Allen M. Costa & Daniel M. Bear & Jing Wu & David A. Harmin & Mike Laptewicz & Kellie Barbara-Haley & Scott Kuersten & Eirene Markenscoff-Papadimitriou, 2010. "Widespread transcription at neuronal activity-regulated enhancers," Nature, Nature, vol. 465(7295), pages 182-187, May.
    6. Robin Andersson & Claudia Gebhard & Irene Miguel-Escalada & Ilka Hoof & Jette Bornholdt & Mette Boyd & Yun Chen & Xiaobei Zhao & Christian Schmidl & Takahiro Suzuki & Evgenia Ntini & Erik Arner & Eivi, 2014. "An atlas of active enhancers across human cell types and tissues," Nature, Nature, vol. 507(7493), pages 455-461, March.
    7. Yafei Yin & J. Yuyang Lu & Xuechun Zhang & Wen Shao & Yanhui Xu & Pan Li & Yantao Hong & Li Cui & Ge Shan & Bin Tian & Qiangfeng Cliff Zhang & Xiaohua Shen, 2020. "U1 snRNP regulates chromatin retention of noncoding RNAs," Nature, Nature, vol. 580(7801), pages 147-150, April.
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