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Repression of genes by DNA methylation depends on CpG density and promoter strength: evidence for involvement of a methyl‐CpG binding protein.
Open accessAbstract
Repression of transcription from densely methylated genes can be mediated by the methyl-CpG binding protein MeCP-1 (Boyes and Bird, 1991). Here we have investigated the effect of methylation on genes with a low density of methyl-CpG. We found that sparse methylation could repress transfected genes completely, but the inhibition was fully overcome by the presence in cis of an SV40 enhancer. Densely methylated genes, however, could not be reactivated by the enhancer. In vitro studies showed that the sparsely methylated genes bound weakly to MeCP-1 and that binding interfered with transcription. In the absence of available MeCP-1, methylation had minimal effects on transcription. From these and other results we propose that sparsely methylated genes form an unstable complex with MeCP-1 which prevents transcription when the promoter is weak. This complex can be disrupted by a strong promoter, thereby allowing the methylated gene to be transcribed.
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“DNA methylation (5-methylcytosine or 5mC) is associated with gene repression (16) and can disrupt the binding of many TFs (17, 18).”
From Hepatocyte Nuclear Factor 4‐Alpha Is Essential for the Active Epigenetic State at Enhancers in Mouse Liver (2019) · cites this paper as [16]
In the citing paper
“Our finding that targeted DNA methylation outside of annotated CGIs can lead to robust memorized gene silencing extends the canonical model of methylation-based gene silencing, which posits that a high density of CpG methylation is a requirement for stable propagation of silencing (Boyes and Bird, 1992).”
From Genome-wide programmable transcriptional memory by CRISPR-based epigenome editing (2021) · cites this paper as Boyes and Bird, 1992
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CpG-rich islands and the function of DNA methylation
Bird, A. P. (1986) · Nature · doi:10.1038/321209a0 · Cited by 3,777
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Methylation and expression of neurofilament genes in tissues and in cell lines of the mouse
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TET2 catalyzes active DNA demethylation of the Sry promoter and enhances its expression
Okashita, N., Kuroki, S., Maeda, R., & Tachibana, M. (2019) · Scientific Reports · doi:10.1038/s41598-019-50058-7 · Cited by 13
Repair of DNA lesions in chromosomal DNA
Fousteri, M. I., van Hoffen, A., Vargova, H., & Mullenders, L. H. F. (2005) · DNA repair · doi:10.1016/j.dnarep.2005.04.011 · Cited by 11
Yang, X., Nakao, Y., Pater, M. M., Tang, S.-C., & Pater, A. (1997) · Journal of Cellular Biochemistry · doi:10.1002/(sici)1097-4644(19970901)66:3 · Cited by 19
CpG Islands: A Historical Perspective
Antequera, F., & Bird, A. P. (2018) · Methods in molecular biology · doi:10.1007/978-1-4939-7768-0_1 · Cited by 14
“CGIs could not be reactivated even by strong enhancers [52, 53].”
BackgroundSelf-citationNatural and artificial routes to pluripotency
Krueger, W. H., Swanson, L. C., Tanasijevic, B., & Rasmussen, T. P. (2010) · The International Journal of Developmental Biology · doi:10.1387/ijdb.103199wk · Cited by 16
Shao, W. (1997) · Journal of Biomedical Sciences · doi:10.1007/bf02255592 · Cited by 13
Metabolic stress induces modifications in the epigenetic program of preimplantation bovine embryos
Tremblay, R., Dufort, I., & Sirard, M. (2017) · Molecular Reproduction and Development · doi:10.1002/mrd.22941 · Cited by 14
“The intensity of gene repression was also reported to be proportional to the density of methylation in specific cases (Boyes & Bird, 1992), but in our study, CpG islands of different lengths and densities were not differentially affected by the glucose treatment.”
BackgroundKAISO inhibition: an atomic insight
Chikan, N. A., & Vipperla, B. (2014) · Journal of Biomolecular Structure and Dynamics · doi:10.1080/07391102.2014.974072 · Cited by 12
“…a series of DNA–protein and protein–protein interactions that begins with the binding of methyl-CpG binding proteins (MBPs), which act as intermediates between the transcriptional machinery and methylated DNA (Boyes & Bird, 1992; Jones et al., 1998; Ng et al., 1999; Valinluck et al., 2004).”
BackgroundSilencing and Activation of Embryonic Globin Gene Expression
Ginder, G. D., Singal, R., Little, J. A., Dempsey, N., Ferris, R. C., & Wang, S. Z. (1998) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1998.tb10464.x · Cited by 10
“As such, MeCP-1 or the analogous factor, MeCPC, which we detect in primary avian erythroid cells and which is likely responsible for the strong suppression of transcription of the methylated ρ-gene promoter, may not be able to bind effectively to the γ-globin gene promoter.(17) Nonetheless, DNA methylation has been im…”
BackgroundMethodInfluentialEyes on DNA methylation: current evidence for DNA methylation in ocular development and disease
Otteson, D. C. (2011) · Journal of ocular biology, diseases, and informatics · doi:10.1007/s12177-012-9078-x · Cited by 12
“containing a single methylated site, although the efficacy of repression is directly correlated to methylation density [76].”
BackgroundMouse embryonic stem cells induce targeted DNA demethylation within human MAGE-A1 transgenes
Loriot, A., Sterpin, C., de Backer, O., & Smet, C. D. (2008) · Epigenetics · doi:10.4161/epi.3.1.5411 · Cited by 11
Metadata
- Authors
- Boyes, J., & Bird, A.
- Affiliations
- Research Institute of Molecular Pathology (AT)
- Venue
- The EMBO Journal
- Published
- 1992-01-01
- Volume
- 11
- Issue
- 1
- Pages
- 327-333
- ISSN
- 0261-4189 (ISSN-L)
- 1460-2075
- PMC
- PMC556453
- OpenAlex
- W1821654469
- Cited by
- 471
- References
- 0
- Citations by year
- 2026: 3 · 2025: 8 · 2024: 7 · 2023: 4 · 2022: 12 · 2021: 8 · 2020: 7 · 2019: 10 · 2018: 10 · 2017: 12 · 2016: 10 · 2015: 6 · 2014: 14 · 2013: 18 · 2012: 8
- FWCI
- 9.92
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- The EMBO Journal (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Syndromes and Imprinting
- Keywords
- DNA methylation, transcriptional repression, CpG density, promoter strength, methyl-CpG binding proteins, SV40 enhancer, gene reactivation, transcriptional silencing
- MeSH terms
- Animals, Binding Sites, DNA-Binding Proteins, Gene Expression Regulation, Globins, Methylation, Models, Genetic, Promoter Regions, Genetic, Simian virus 40, Transcription, Genetic, Transfection, DNA Modification Methylases, DNA-Cytosine Methylases, Mice
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