Transcription Elongation Can Affect Genome 3D Structure
Open accessAbstract
How transcription affects genome 3D organization is not well understood. We found that during influenza A (IAV) infection, rampant transcription rapidly reorganizes host cell chromatin interactions. These changes occur at the ends of highly transcribed genes, where global inhibition of transcription termination by IAV NS1 protein causes readthrough transcription for hundreds of kilobases. In these readthrough regions, elongating RNA polymerase II disrupts chromatin interactions by inducing cohesin displacement from CTCF sites, leading to locus decompaction. Readthrough transcription into heterochromatin regions switches them from the inert (B) to the permissive (A) chromatin compartment and enables transcription factor binding. Data from non-viral transcription stimuli show that transcription similarly affects cohesin-mediated chromatin contacts within gene bodies. Conversely, inhibition of transcription elongation allows cohesin to accumulate at previously transcribed intragenic CTCF sites and to mediate chromatin looping and compaction. Our data indicate that transcription elongation by RNA polymerase II remodels genome 3D architecture.
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In read-through regions, elongating RNA Pol II displaces cohesin from CTCF sites thus eliminating chromatin loops and locally decompacting chromatin.
“Finally, read‐through transcription can also affect the genome 3D structure: In read‐through regions, elongating RNA Pol II displaces cohesin from CTCF sites thus eliminating chromatin loops and locally decompacting chromatin (Heinz et al, 2018).”
From RNA polymerase II speed: a key player in controlling and adapting transcriptome composition (2021) · cites this paper as Heinz et al, 2018
Transcription at stimulus-response genes was shown to disrupt chromatin loops, potentially through destabilising cohesin association with the chromatin fibre by RNAP machinery.
“For example, transcription at stimulus–response genes was shown to disrupt chromatin loops [387, 388], potentially through destabilising cohesin association with the chromatin fibre by RNAP machinery [388].”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [388]
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A chromosome-scale genome assembly and karyotype of the ctenophore <i>Hormiphora californensis</i>
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Duttke, S. H., Montilla-Perez, P., Chang, M. W., Li, H., Chen, H., Carrette, L. L. G., Guglielmo, G. D., George, O., Palmer, A. A., Benner, C., et al. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.858427 · Cited by 26 · see citing works
Self-citationEstrada‐Capetillo, L., Aragoneses‐Fenoll, L., Domínguez‐Soto, Á., Fuentelsaz‐Romero, S., Nieto, C., Simón‐Fuentes, M., Alonso, B., Portolés, P., Corbí, A. L., Rojo, J. M., et al. (2021) · European Journal of Immunology · doi:10.1002/eji.202048806 · Cited by 22 · see citing works
- Authors
- Heinz, S., Texari, L., Hayes, M. G. B., Urbanowski, M., Chang, M. W., Givarkes, N., Rialdi, A., White, K. M., Albrecht, R. A., Pache, L., Marazzi, I., García-Sastre, A., Shaw, M. L., & Benner, C.
- Affiliations
- University of California San Diego (US)
- Icahn School of Medicine at Mount Sinai (US)
- Sanford Burnham Prebys Medical Discovery Institute (US)
- Corresponding author
- Heinz, Sven
- Benner, Christopher
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2018-09
- Volume
- 174
- Issue
- 6
- Pages
- 1522-1536.e22
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC6130916
- OpenAlex
- W2888200508
- Cited by
- 453
- References
- 64
- Citations by year
- 2026: 27 · 2025: 48 · 2024: 71 · 2023: 54 · 2022: 66 · 2021: 73 · 2020: 67 · 2019: 41 · 2018: 5
- FWCI
- 16.90
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- NIH-NIAID (U19 AI106754)
- Pilot Project Grant
- SNSF Advanced Postdoc Mobility fellowship (P300PA_164714)
- Salk Institute’s NGS Core Facility
- NIH-NCI CCSG (P30 014195)
- Chapman Foundation
- Helmsley Charitable Trust
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nuclear Structure and Function
- Keywords
- transcription elongation, chromatin interactions, influenza A virus, NS1 protein, read-through transcription, RNA polymerase II, cohesin, CTCF, heterochromatin, chromatin looping, transcription termination
- MeSH terms
- CCCTC-Binding Factor, Cohesins, Binding Sites, Carrier Proteins, Cell Line, Chromatin, Chromosomal Proteins, Non-Histone, Flavonoids, Humans, Macrophages, Nuclear Proteins, Piperidines, Protein Binding, Proto-Oncogene Proteins, RNA Polymerase II, Transcription, Genetic, Genome, Human, Interferon-beta, Viral Nonstructural Proteins, Cell Cycle Proteins, RNA Interference, RNA, Small Interfering, Influenza A Virus, H5N1 Subtype
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