Cited by 320Genetic Syndromes and ImprintingGenomics and Chromatin DynamicsEpigenetics and DNA Methylation

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CTCF maintains differential methylation at the Igf2/H19 locus

Schoenherr, Christopher J., Levorse, John M., Tilghman, Shirley M.·2003·Nature Genetics

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Abstract

Genomic imprinting relies on establishing and maintaining the parental-specific methylation of DNA elements that control the differential expression of maternal and paternal alleles. Although the essential DNA methyltransferases have been discovered, proteins that regulate the sequence-specific establishment and maintenance of allelic methylation have not been identified. One candidate regulator of methylation, the zinc-finger protein CTCF, binds to the imprinting control region (ICR) of the genes Igf2 (encoding insulin-like growth factor 2) and H19 (fetal liver mRNA; refs. 1,2). The unmethylated maternal ICR is a chromatin boundary that prevents distant enhancers from activating Igf2 (refs. 3-6). In vitro experiments have suggested that CTCF mediates boundary activity of the maternal ICR, and that methylation of the paternal ICR abolishes this activity by preventing CTCF binding. Using mice with point mutations in all four CTCF sites in the ICR, we show that maternally transmitted mutant ICRs in neonatal mice acquire a substantial but heterogeneous degree of methylation. Mutant ICRs in oocytes and blastocysts are not methylated, however, indicating that binding of CTCF is not required to establish the unmethylated ICR during oogenesis. We also show that the mutant ICR lacks enhancer-blocking activity, as the expression of Igf2 is activated on mutant maternal chromosomes. Conversely, maternal H19 expression is reduced, suggesting a positive role for CTCF in the transcription of that gene. This study constitutes the first in vivo demonstration of the multiple functions of CTCF in an ICR.

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Authors: Schoenherr, C. J., Levorse, J. M., & Tilghman, S. M.
Affiliations: University of Illinois Urbana-Champaign (US)
Howard Hughes Medical Institute (US)
Corresponding author: Schoenherr, Christopher J.
Tilghman, Shirley M.
ORCID: Schoenherr, Christopher J.
Levorse, John M.
Venue: Nature Genetics
Publisher: Springer Science and Business Media LLC
Published: 2002-12-02
Volume: 33
Issue: 1
Pages: 66-69
ISSN: 1061-4036 (ISSN-L)
1546-1718
DOI: 10.1038/ng1057
OpenAlex: W2036636377
Cited by: 320
References: 26
Citations by year: 2026: 3 · 2025: 5 · 2024: 4 · 2023: 4 · 2022: 6 · 2021: 7 · 2020: 10 · 2019: 7 · 2018: 7 · 2017: 9 · 2016: 10 · 2015: 14 · 2014: 9 · 2013: 15 · 2012: 22
FWCI: 13.84
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Nature Genetics (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Syndromes and Imprinting
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
Keywords: CTCF, genomic imprinting, Igf2/H19 locus, imprinting control regions, DNA methylation, chromatin boundaries, enhancer blocking, maternal allele, oogenesis, blastocyst, IGF2 expression, zinc finger proteins
MeSH terms: CCCTC-Binding Factor, Alleles, Amino Acid Sequence, Animals, Animals, Newborn, Binding Sites, Blastocyst, Cell Line, DNA, DNA-Binding Proteins, Female, Gene Expression Regulation, Insulin-Like Growth Factor II, Male, Molecular Sequence Data, Mutation, Oocytes, Protein Binding, Repressor Proteins, RNA, Messenger, Sulfites, Transcription Factors, Genomic Imprinting, DNA Methylation, RNA, Untranslated, Mice, RNA, Long Noncoding

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CTCF maintains differential methylation at the Igf2/H19 locus

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