Uncoupling antisense-mediated silencing and DNA methylation in the imprinted Gnas cluster
Open accessAbstract
There is increasing evidence that non-coding macroRNAs are major elements for silencing imprinted genes, but their mechanism of action is poorly understood. Within the imprinted Gnas cluster on mouse chromosome 2, Nespas is a paternally expressed macroRNA that arises from an imprinting control region and runs antisense to Nesp, a paternally repressed protein coding transcript. Here we report a knock-in mouse allele that behaves as a Nespas hypomorph. The hypomorph mediates down-regulation of Nesp in cis through chromatin modification at the Nesp promoter but in the absence of somatic DNA methylation. Notably there is reduced demethylation of H3K4me3, sufficient for down-regulation of Nesp, but insufficient for DNA methylation; in addition, there is depletion of the H3K36me3 mark permissive for DNA methylation. We propose an order of events for the regulation of a somatic imprint on the wild-type allele whereby Nespas modulates demethylation of H3K4me3 resulting in repression of Nesp followed by DNA methylation. This study demonstrates that a non-coding antisense transcript or its transcription is associated with silencing an overlapping protein-coding gene by a mechanism independent of DNA methylation. These results have broad implications for understanding the hierarchy of events in epigenetic silencing by macroRNAs.
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Antisense RNA can play a role in the mechanics of imprinting.
“Because antisense RNA can play a role in the mechanics of imprinting (53), this observation is of some note.”
From Individual common variants exert weak effects on the risk for autism spectrum disorders (2012) · cites this paper as [53]
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- Authors
- Williamson, C. M., Ball, S. T., Dawson, C., Mehta, S., Beechey, C. V., Fray, M., Teboul, L., Dear, T. N., Kelsey, G., & Peters, J.
- Affiliations
- Medical Research Council (GB)
- Babraham Institute (GB)
- Mary Lyon Centre at MRC Harwell (GB)
- Corresponding author
- Peters, Jo
- Venue
- PLoS Genetics
- Publisher
- Public Library of Science (PLoS)
- Published
- 2011-03-24
- Volume
- 7
- Issue
- 3
- Pages
- e1001347
- ISSN
- 1553-7390 (ISSN-L)
- 1553-7404
- PMC
- PMC3063750
- OpenAlex
- W2030487003
- Cited by
- 100
- References
- 49
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 1 · 2023: 4 · 2022: 4 · 2021: 10 · 2020: 3 · 2019: 6 · 2018: 4 · 2017: 4 · 2016: 9 · 2015: 9 · 2014: 5 · 2013: 15 · 2012: 13
- FWCI
- 8.18
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Genetics (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, other-oa)
- PubMed Central (publishedVersion, other-oa)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Funders
- Directorate for Biological Sciences
- Medical Research Council
- Biotechnology and Biological Sciences Research Council
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Syndromes and Imprinting
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer-related molecular mechanisms research
- Keywords
- genomic imprinting, NESP, non-coding RNA, DNA methylation, H3K36me3, chromatin modification, epigenetic silencing, paternally expressed genes, imprinting control regions, cis-regulation
- MeSH terms
- Alleles, Animals, Chromogranins, Female, Gene Expression Regulation, Histones, Male, Mutation, RNA, Antisense, Gene Targeting, Genomic Imprinting, DNA Methylation, GTP-Binding Protein alpha Subunits, Gs, Gene Silencing, Gene Order, Animals, Genetically Modified, Mice
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