Transcription-dependent cohesin repositioning rewires chromatin loops in cellular senescence
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Abstract
Senescence is a state of stable proliferative arrest, generally accompanied by the senescence-associated secretory phenotype, which modulates tissue homeostasis. Enhancer-promoter interactions, facilitated by chromatin loops, play a key role in gene regulation but their relevance in senescence remains elusive. Here, we use Hi-C to show that oncogenic RAS-induced senescence in human diploid fibroblasts is accompanied by extensive enhancer-promoter rewiring, which is closely connected with dynamic cohesin binding to the genome. We find de novo cohesin peaks often at the 3′ end of a subset of active genes. RAS-induced de novo cohesin peaks are transcription-dependent and enriched for senescence-associated genes, exemplified by IL1B , where de novo cohesin binding is involved in new loop formation. Similar IL1B induction with de novo cohesin appearance and new loop formation are observed in terminally differentiated macrophages, but not TNFα-treated cells. These results suggest that RAS-induced senescence represents a cell fate determination-like process characterised by a unique gene expression profile and 3D genome folding signature, mediated in part through cohesin redistribution on chromatin.
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Changes in the higher-order structure of chromatin contribute to the development of SASP or SASP-like inflammatory gene expression.
“Recent studies by our group and others have suggested that changes in the higher-order structure of chromatin contribute to the development of SASP or SASP-like inflammatory gene expression (11, 19–22).”
From Chromatin conformational changes at human satellite II contribute to the senescence phenotype in the tumor microenvironment (2023) · cites this paper as [20]
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Dynamic enhancer interactome promotes senescence and agingPreprint
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Mosaic Regulation of Stress Pathways Underlies Senescent Cell HeterogeneityPreprint
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Senescence-Associated Chromatin Rewiring Promotes Inflammation and Transposable Element ActivationPreprint
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Valency-driven division of labor balances chromatin compaction and structural plasticityPreprint
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From compartments to gene loops: Functions of the 3D genome in the human brainPreprint
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Determining the Compaction State of Genes Using DNA FISH
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The impact of 3D chromatin remodeling on cellular senescence and aging
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- Authors
- Olan, I., Parry, A. J., Schoenfelder, S., Narita, M., Ito, Y., Chan, A. S. L., Slater, G. S. C., Bihary, D., Bando, M., Shirahige, K., Kimura, H., Samarajiwa, S. A., Fraser, P., & Narita, M.
- Affiliations
- University of Cambridge (GB)
- Babraham Institute (GB)
- Tokyo Institute of Technology (JP)
- The University of Tokyo (JP)
- Florida State University (US)
- Corresponding author
- Narita, Masako
- Fraser, Peter
- Narita, Masashi
- ORCID
- Venue
- Nature Communications
- Published
- 2020-11-27
- Volume
- 11
- Issue
- 1
- Pages
- 6049-6049
- ISSN
- 2041-1723 (ISSN-L)
- PMC
- PMC7695716
- OpenAlex
- W3108031567
- Cited by
- 76
- References
- 76
- Citations by year
- 2026: 8 · 2025: 11 · 2024: 21 · 2023: 13 · 2022: 9 · 2021: 11 · 2020: 3
- FWCI
- 2.92
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Nature Communications (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Institutional Repositories DataBase (IRDB) (submittedVersion)
- Tokyo Tech Research Repository (Tokyo Institute of Technology) (submittedVersion)
- Apollo (University of Cambridge) (submittedVersion)
- Apollo (University of Cambridge) (submittedVersion, cc-by)
- Apollo
- Apollo (cc-by)
- Funders
- Wellcome Trust (105367/Z/14/Z, 215912/Z/19/Z)
- RCUK | Biotechnology and Biological Sciences Research Council (BB/J004480/1, BB/S013466/1)
- RCUK | Medical Research Council (MR/T016787/1, MC_UU_12022/10, MR/L007150/1, MR/M013049/1)
- Babraham Institute (Career Progression Fellowship)
- Cancer Research UK (C9545/A29580)
- MEXT | Japan Society for the Promotion of Science (15H05976, JP17H01417, JP18H05527)
- MEXT | JST | Core Research for Evolutional Science and Technology (JPMJCR16G1)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Health Sciences › Medicine › Physiology › Telomeres, Telomerase, and Senescence
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
- Keywords
- cellular senescence, cohesin, chromatin looping, enhancer-promoter interactions, 3D genome organization, IL1B, macrophage differentiation, senescence-associated secretory phenotype, gene expression regulation, Hi-C
- MeSH terms
- CCCTC-Binding Factor, Cohesins, Cell Differentiation, Cell Line, Chromatin, Chromosomal Proteins, Non-Histone, Enhancer Elements, Genetic, Gene Expression Regulation, Humans, Interleukin-1, Macrophages, Promoter Regions, Genetic, Protein Binding, Transcription, Genetic, Tumor Necrosis Factor-alpha, Genome, Cellular Senescence, ras Proteins, Cell Cycle Proteins, Genetic Loci
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