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Highly rearranged chromosomes reveal uncoupling between genome topology and gene expression
Open accessAbstract
Chromatin topology is intricately linked to gene expression, yet its functional requirement remains unclear. Here, we comprehensively assessed the interplay between genome topology and gene expression using highly rearranged chromosomes (balancers) spanning ~75% of the Drosophila genome. Using transheterozyte (balancer/wild-type) embryos, we measured allele-specific changes in topology and gene expression in cis, while minimizing trans effects. Through genome sequencing, we resolved eight large nested inversions, smaller inversions, duplications and thousands of deletions. These extensive rearrangements caused many changes to chromatin topology, disrupting long-range loops, topologically associating domains (TADs) and promoter interactions, yet these are not predictive of changes in expression. Gene expression is generally not altered around inversion breakpoints, indicating that mis-appropriate enhancer-promoter activation is a rare event. Similarly, shuffling or fusing TADs, changing intra-TAD connections and disrupting long-range inter-TAD loops does not alter expression for the majority of genes. Our results suggest that properties other than chromatin topology ensure productive enhancer-promoter interactions.
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“the considerable TAD re-arrangements observed in Drosophila balancer chromosomes compared with their wild-type counterparts result in changes in the expression of only ~ 10% of genes [449].”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [449]
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“Third, biochemical annotations fail to specify which gene(s) a putative enhancer regulates, let alone the degree of activation conferred78,79.”
From Towards a comprehensive catalogue of validated and target-linked human enhancers (2020) · cites this paper as [78]
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Metadata
- Authors
- Ghavi-Helm, Y., Jankowski, A., Meiers, S., Viales, R. R., Korbel, J. O., & Furlong, E. E. M.
- Affiliations
- Lyon 1 Université (FR)
- European Molecular Biology Laboratory (DE)
- Corresponding author
- Ghavi-Helm, Yad
- Korbel, Jan O.
- Furlong, Eileen E. M.
- ORCID
- Venue
- Nature Genetics
- Published
- 2019-07-15
- Volume
- 51
- Issue
- 8
- Pages
- 1272-1282
- ISSN
- 1061-4036 (ISSN-L)
- 1546-1718
- PMC
- PMC7116017
- OpenAlex
- W2958578938
- Cited by
- 354
- References
- 57
- Citations by year
- 2026: 16 · 2025: 33 · 2024: 41 · 2023: 54 · 2022: 60 · 2021: 74 · 2020: 56 · 2019: 19
- FWCI
- 17.94
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature Genetics (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- HAL (submittedVersion)
- Funders
- Nature
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Chromosomal and Genetic Variations
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
- Keywords
- chromatin topology, gene expression, balancer chromosomes, chromosomal inversions, topologically associating domains, enhancer-promoter interactions, cis effect, Drosophila, chromosomal duplication, chromosomal deletion
- MeSH terms
- Animals, Chromatin, Chromosome Mapping, Drosophila melanogaster, Enhancer Elements, Genetic, Female, Gene Expression Regulation, Male, Promoter Regions, Genetic, Gene Rearrangement, Genome, Insect, Chromosomes, Insect
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