Igf2 adult-specific skeletal muscle enhancer activity revealed in mice with intergenic CTCF boundary deletion

PLoS Genet. 2025 Aug 29;21(8):e1011834. doi: 10.1371/journal.pgen.1011834. eCollection 2025 Aug.

Abstract

Precise, monoallelic expression of imprinted genes is governed by cis regulatory elements called imprinting control regions (ICRs) and enhancer-promoter (E-P) interactions shaped by local chromatin architecture. The Igf2/H19 locus employs allele-specific CTCF binding at the ICR to instruct enhancer accessibility to maternal H19 and paternal Igf2 promoters. Here, we investigate the CTCF-bound centrally conserved domain (CCD), intergenic to H19 and Igf2, and an adjacent widely expressed lncRNA. Using transgenic mice, deletion alleles reinforced CCD as a neonatal muscle-specific repressor of maternal Igf2. However, deletion of the abutting lncRNA did not affect Igf2 levels. Unexpectedly, in adult skeletal muscle where Igf2 is normally repressed, absence of CCD resulted in remarkable, high-level activation of Igf2 from both parental alleles. Through multimodal chromatin analyses, we identified a conserved putative adult skeletal muscle enhancer (PaSME) insulated between chromatin domains at ICR and CCD. We propose that removal of CCD allows PaSME to drive robust abnormal Igf2 activation on both alleles in adult skeletal muscle. Thus, we uncover CCD as a developmental biallelic muscle-specific repressor, adding a new layer of architectural regulation to the extensively studied Igf2/H19 locus.

MeSH terms

  • Alleles
  • Animals
  • CCCTC-Binding Factor* / genetics
  • Chromatin / genetics
  • Enhancer Elements, Genetic* / genetics
  • Gene Expression Regulation, Developmental
  • Genomic Imprinting / genetics
  • Insulin-Like Growth Factor II* / genetics
  • Insulin-Like Growth Factor II* / metabolism
  • Mice
  • Mice, Transgenic
  • Muscle, Skeletal* / growth & development
  • Muscle, Skeletal* / metabolism
  • Promoter Regions, Genetic
  • RNA, Long Noncoding / genetics

Substances

  • Insulin-Like Growth Factor II
  • CCCTC-Binding Factor
  • IGF2 protein, mouse
  • Ctcf protein, mouse
  • RNA, Long Noncoding
  • H19 long non-coding RNA
  • Chromatin