Genome-wide analysis of the interplay between chromatin-associated RNA and 3D genome organization in human cells

Riccardo Calandrelli, Xingzhao Wen, John Lalith Charles Richard, Zhifei Luo, Tri C. Nguyen, Chien-Ju Chen, Zhijie Qi, Shuanghong Xue, Weizhong Chen, Zhangming Yan, Weixin Wu, Kathia Zaleta-Rivera, Rong Hu, Miao Yu, Yuchuan Wang, Wenbo Li, Jian Ma, Bing Ren and Sheng Zhong ()
Additional contact information
Riccardo Calandrelli: University of California San Diego
Xingzhao Wen: University of California San Diego
John Lalith Charles Richard: University of California San Diego
Zhifei Luo: University of California San Diego
Tri C. Nguyen: University of California San Diego
Chien-Ju Chen: University of California San Diego
Zhijie Qi: University of California San Diego
Shuanghong Xue: University of California San Diego
Weizhong Chen: University of California San Diego
Zhangming Yan: University of California San Diego
Weixin Wu: University of California San Diego
Kathia Zaleta-Rivera: University of California San Diego
Rong Hu: University of California San Diego
Miao Yu: Ludwig Institute for Cancer Research
Yuchuan Wang: Carnegie Mellon University
Wenbo Li: University of Texas Health Science Center
Jian Ma: Carnegie Mellon University
Bing Ren: University of California San Diego
Sheng Zhong: University of California San Diego

Nature Communications, 2023, vol. 14, issue 1, 1-14

Abstract: Abstract The interphase genome is dynamically organized in the nucleus and decorated with chromatin-associated RNA (caRNA). It remains unclear whether the genome architecture modulates the spatial distribution of caRNA and vice versa. Here, we generate a resource of genome-wide RNA-DNA and DNA-DNA contact maps in human cells. These maps reveal the chromosomal domains demarcated by locally transcribed RNA, hereafter termed RNA-defined chromosomal domains. Further, the spreading of caRNA is constrained by the boundaries of topologically associating domains (TADs), demonstrating the role of the 3D genome structure in modulating the spatial distribution of RNA. Conversely, stopping transcription or acute depletion of RNA induces thousands of chromatin loops genome-wide. Activation or suppression of the transcription of specific genes suppresses or creates chromatin loops straddling these genes. Deletion of a specific caRNA-producing genomic sequence promotes chromatin loops that straddle the interchromosomal target sequences of this caRNA. These data suggest a feedback loop where the 3D genome modulates the spatial distribution of RNA, which in turn affects the dynamic 3D genome organization.

Date: 2023
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DOI: 10.1038/s41467-023-42274-7

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