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Three-dimensional organization of chromatin associated RNAs and their role in chromatin architecture in human cells

View ORCID ProfileRiccardo Calandrelli, Xingzhao Wen, Tri C. Nguyen, Chien-Ju Chen, Zhijie Qi, Weizhong Chen, Zhangming Yan, Weixin Wu, Kathia Zaleta-Rivera, Rong Hu, Miao Yu, Yuchuan Wang, View ORCID ProfileJian Ma, Bing Ren, View ORCID ProfileSheng Zhong
doi: https://doi.org/10.1101/2021.06.10.447969
Riccardo Calandrelli
1Department of Bioengineering, University of California San Diego, La Jolla, CA, USA
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  • ORCID record for Riccardo Calandrelli
Xingzhao Wen
2Bioinformatics and Systems Biology Program, University of California San Diego, La Jolla, CA, USA
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Tri C. Nguyen
1Department of Bioengineering, University of California San Diego, La Jolla, CA, USA
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Chien-Ju Chen
2Bioinformatics and Systems Biology Program, University of California San Diego, La Jolla, CA, USA
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Zhijie Qi
1Department of Bioengineering, University of California San Diego, La Jolla, CA, USA
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Weizhong Chen
1Department of Bioengineering, University of California San Diego, La Jolla, CA, USA
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Zhangming Yan
1Department of Bioengineering, University of California San Diego, La Jolla, CA, USA
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Weixin Wu
1Department of Bioengineering, University of California San Diego, La Jolla, CA, USA
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Kathia Zaleta-Rivera
1Department of Bioengineering, University of California San Diego, La Jolla, CA, USA
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Rong Hu
3Department of Cellular and Molecular Medicine, Center for Epigenomics, University of California San Diego, La Jolla, CA, USA
4Ludwig Institute for Cancer Research, La Jolla, CA, USA
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Miao Yu
4Ludwig Institute for Cancer Research, La Jolla, CA, USA
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Yuchuan Wang
5Computational Biology Department, School of Computer Science, Carnegie Mellon University, Pittsburgh, PA, USA
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Jian Ma
5Computational Biology Department, School of Computer Science, Carnegie Mellon University, Pittsburgh, PA, USA
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Bing Ren
3Department of Cellular and Molecular Medicine, Center for Epigenomics, University of California San Diego, La Jolla, CA, USA
4Ludwig Institute for Cancer Research, La Jolla, CA, USA
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Sheng Zhong
1Department of Bioengineering, University of California San Diego, La Jolla, CA, USA
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  • For correspondence: szhong@ucsd.edu
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Abstract

Chromatin-associated RNA (caRNA) is a vital component of the interphase nucleus; yet its distribution and role in the three-dimensional (3D) genome organization and function remain poorly understood. Here, we map caRNA’s spatial distribution on the 3D genome in human embryonic stem cells, fibroblasts, and myelogenous leukemia cells. We find that the relative abundance of trans-acting caRNA reflects the functional nuclear compartmentalization of the 3D genome, and the caRNA’s sequence features are predictive of its spatial localization. We observe extensive caRNA-genome interactions that span several hundred kilobases to several megabases. These caRNA domains correlate with chromatin loops and enhancer-promoter interactions. We report a tradeoff of caRNA’s promotive and suppressive roles to chromatin interactions. As a result, caRNA promotes chromatin interactions outside the anchors of chromatin loops, whereas caRNA exhibits an overall suppressive impact to chromatin interactions between loop anchors. Furthermore, caRNA suppresses chromatin loops’ number and strengths genome-wide, and this suppression depends on electric charge-mediated RNA interactions. These results reveal caRNA’s multifaced role in regulating 3D chromatin organization and highlight caRNA’s ability to modulate chromatin looping.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted July 14, 2021.
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Three-dimensional organization of chromatin associated RNAs and their role in chromatin architecture in human cells
Riccardo Calandrelli, Xingzhao Wen, Tri C. Nguyen, Chien-Ju Chen, Zhijie Qi, Weizhong Chen, Zhangming Yan, Weixin Wu, Kathia Zaleta-Rivera, Rong Hu, Miao Yu, Yuchuan Wang, Jian Ma, Bing Ren, Sheng Zhong
bioRxiv 2021.06.10.447969; doi: https://doi.org/10.1101/2021.06.10.447969
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Three-dimensional organization of chromatin associated RNAs and their role in chromatin architecture in human cells
Riccardo Calandrelli, Xingzhao Wen, Tri C. Nguyen, Chien-Ju Chen, Zhijie Qi, Weizhong Chen, Zhangming Yan, Weixin Wu, Kathia Zaleta-Rivera, Rong Hu, Miao Yu, Yuchuan Wang, Jian Ma, Bing Ren, Sheng Zhong
bioRxiv 2021.06.10.447969; doi: https://doi.org/10.1101/2021.06.10.447969

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