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


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
16 10 2023
Historique:
received: 17 05 2023
accepted: 05 10 2023
medline: 23 10 2023
pubmed: 17 10 2023
entrez: 16 10 2023
Statut: epublish

Résumé

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.

Identifiants

pubmed: 37845234
doi: 10.1038/s41467-023-42274-7
pii: 10.1038/s41467-023-42274-7
pmc: PMC10579264
doi:

Substances chimiques

Chromatin 0
RNA 63231-63-0
DNA 9007-49-2
RNA, Small Nuclear 0

Types de publication

Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

6519

Subventions

Organisme : NIGMS NIH HHS
ID : R01 GM136922
Pays : United States
Organisme : NHLBI NIH HHS
ID : U01 HL156059
Pays : United States

Informations de copyright

© 2023. Springer Nature Limited.

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Auteurs

Riccardo Calandrelli (R)

Shu Chien-Gene Lay Department of Bioengineering, University of California San Diego, La Jolla, CA, USA.

Xingzhao Wen (X)

Bioinformatics and Systems Biology Program, University of California San Diego, La Jolla, CA, USA.

John Lalith Charles Richard (JL)

Shu Chien-Gene Lay Department of Bioengineering, University of California San Diego, La Jolla, CA, USA.

Zhifei Luo (Z)

Shu Chien-Gene Lay Department of Bioengineering, University of California San Diego, La Jolla, CA, USA.

Tri C Nguyen (TC)

Shu Chien-Gene Lay Department of Bioengineering, University of California San Diego, La Jolla, CA, USA.

Chien-Ju Chen (CJ)

Bioinformatics and Systems Biology Program, University of California San Diego, La Jolla, CA, USA.

Zhijie Qi (Z)

Shu Chien-Gene Lay Department of Bioengineering, University of California San Diego, La Jolla, CA, USA.

Shuanghong Xue (S)

Shu Chien-Gene Lay Department of Bioengineering, University of California San Diego, La Jolla, CA, USA.

Weizhong Chen (W)

Shu Chien-Gene Lay Department of Bioengineering, University of California San Diego, La Jolla, CA, USA.

Zhangming Yan (Z)

Shu Chien-Gene Lay Department of Bioengineering, University of California San Diego, La Jolla, CA, USA.

Weixin Wu (W)

Shu Chien-Gene Lay Department of Bioengineering, University of California San Diego, La Jolla, CA, USA.

Kathia Zaleta-Rivera (K)

Shu Chien-Gene Lay Department of Bioengineering, University of California San Diego, La Jolla, CA, USA.

Rong Hu (R)

Department of Cellular and Molecular Medicine, Center for Epigenomics, University of California San Diego, La Jolla, CA, USA.
Ludwig Institute for Cancer Research, La Jolla, CA, USA.

Miao Yu (M)

Ludwig Institute for Cancer Research, La Jolla, CA, USA.

Yuchuan Wang (Y)

Computational Biology Department, School of Computer Science, Carnegie Mellon University, Pittsburgh, PA, USA.

Wenbo Li (W)

Department of Biochemistry and Molecular Biology, McGovern Medical School, University of Texas Health Science Center, Houston, TX, USA.

Jian Ma (J)

Computational Biology Department, School of Computer Science, Carnegie Mellon University, Pittsburgh, PA, USA.

Bing Ren (B)

Department of Cellular and Molecular Medicine, Center for Epigenomics, University of California San Diego, La Jolla, CA, USA.
Ludwig Institute for Cancer Research, La Jolla, CA, USA.

Sheng Zhong (S)

Shu Chien-Gene Lay Department of Bioengineering, University of California San Diego, La Jolla, CA, USA. szhong@ucsd.edu.

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Classifications MeSH