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Cited by 132Genomics and Chromatin DynamicsChromatin Remodeling and CancerNuclear Structure and Function

Cohesin-dependence of neuronal gene expression relates to chromatin loop length

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Calderon, Lesly, Weiss, Felix D, Beagan, Jonathan A, Oliveira, Marta S, Georgieva, Radina, Wang, Yi-Fang, Carroll, Thomas S, Dharmalingam, Gopuraja +8 more·2022·eLife
DOI 10.7554/elife.76539PMC PMC9106336

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Abstract

Cohesin and CTCF are major drivers of 3D genome organization, but their role in neurons is still emerging. Here, we show a prominent role for cohesin in the expression of genes that facilitate neuronal maturation and homeostasis. Unexpectedly, we observed two major classes of activity-regulated genes with distinct reliance on cohesin in mouse primary cortical neurons. Immediate early genes (IEGs) remained fully inducible by KCl and BDNF, and short-range enhancer-promoter contacts at the IEGs Fos formed robustly in the absence of cohesin. In contrast, cohesin was required for full expression of a subset of secondary response genes characterized by long-range chromatin contacts. Cohesin-dependence of constitutive neuronal genes with key functions in synaptic transmission and neurotransmitter signaling also scaled with chromatin loop length. Our data demonstrate that key genes required for the maturation and activation of primary cortical neurons depend on cohesin for their full expression, and that the degree to which these genes rely on cohesin scales with the genomic distance traversed by their chromatin contacts.

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  • Cohesin depletion significantly suppresses the activation of inducible genes, especially when the enhancer is located at a significant distance from the promoter.

    “At the same time, cohesin depletion significantly suppresses the activation of inducible genes, especially when the enhancer is located at a significant distance from the promoter [120,121,122].”

    From Enhancer Function in the 3D Genome (2023) · cites this paper as [120]

    The Results (pages unavailable) report that a subset of late-response genes failed to reach normal expression after stimulation in cohesin-deficient neurons, and that these genes formed significantly longer chromatin loops. But most immediate-early genes and some late-response genes remained fully inducible. The observed tendency toward longer enhancer–promoter loops specifically did not reach statistical significance, so the claim overstates both the general effect on inducible genes and the evidence for enhancer–promoter distance. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

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Authors
Calderon, L., Weiss, F. D., Beagan, J. A., Oliveira, M. S., Georgieva, R., Wang, Y.-F., Carroll, T. S., Dharmalingam, G., Gong, W., Tossell, K., de Paola, V., Whilding, C., Ungless, M. A., Fisher, A. G., Phillips-Cremins, J. E., & Merkenschlager, M.
Affiliations
  • MRC London Institute of Medical Sciences, Imperial College London
  • Imperial College London (GB)
  • University of Pennsylvania (US)
  • MRC London Institute of Medical Sciences (GB)
  • Institute of Clinical Sciences, Faculty of Medicine, Imperial College
Corresponding author
  • Phillips-Cremins, Jennifer E
  • Merkenschlager, Matthias
ORCID
Venue
eLife
Publisher
eLife Sciences Publications, Ltd
Published
2022-04-26
Volume
11
ISSN
2050-084X (ISSN-L)
DOI
10.7554/elife.76539
PMC
PMC9106336
OpenAlex
W4224929654
Cited by
132
References
21
Citations by year
2026: 20 · 2025: 41 · 2024: 34 · 2023: 24 · 2022: 10 · 2021: 3
FWCI
8.90
Type
journal article
Language
en
Open access
Licence
Locations
  • eLife (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Spiral (Imperial College London) (submittedVersion, cc-by)
Funders
  • Medical Research Council
  • Wellcome Trust (099276/Z/12/Z)
  • European Molecular Biology Organization (ALTF 1047-2012)
  • Human Frontier Science Program (LT00427/2013)
  • National Institutes of Health (1R01-MH120269, 1DP1OD031253, 1R01-NS114226)
  • 4D Nucleome Common Fund (1U01DK127405)
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
cohesin, CTCF, 3D genome organization, chromatin looping, neuronal gene expression, primary cortical neurons, immediate early genes, FOS, enhancer-promoter interactions, long-range chromatin contacts, neuronal maturation, brain-derived neurotrophic factor, KCl stimulation
MeSH terms
CCCTC-Binding Factor, Cohesins, Animals, Chromatin, Chromosomal Proteins, Non-Histone, Neurons, Gene Expression, Cell Cycle Proteins, Mice

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