NF-Y regulates the antisense promoter, bidirectional silencing, and differential epigenetic marks of the Kcnq1 imprinting control region

J Biol Chem. 2004 Dec 10;279(50):52685-93. doi: 10.1074/jbc.M408084200. Epub 2004 Sep 29.

Abstract

Antisense transcription has been shown to be one of the hierarchies that control gene expression in eukaryotes. Recently, we have documented that the mouse Kcnq1 imprinting control region (ICR) harbors bidirectional silencing property, and this feature is linked to an antisense RNA, Kcnq1ot1. In this investigation, using genomic footprinting, we have identified three NF-Y transcription factor binding sites appearing in a methylation-sensitive manner in the Kcnq1ot1 promoter. By employing a dominant negative mutant to the NF-Y transcription factor, we have shown that the NF-Y transcription factor positively regulates antisense transcription. Selective mutation of the conserved nucleotides in the NF-Y binding sites resulted in the loss of antisense transcription. The loss of antisense transcription from the Kcnq1ot1 promoter coincides with an enrichment in the levels of deacetylation and methylation at the lysine 9 residue of histone H3 and DNA methylation at the CpG residues, implying a crucial role for the NF-Y transcription factor in organizing the parent of origin-specific chromatin conformation in the Kcnq1 ICR. Parallel to the loss of antisense transcription, the loss of silencing of the flanking reporter genes was observed, suggesting that NF-Y-mediated Kcnq1ot1 transcription is critical in the bidirectional silencing process of the Kcnq1 ICR. These data highlight the NF-Y transcription factor as a crucial regulator of antisense promoter-mediated bidirectional silencing and the parent of origin-specific epigenetic marks at the Kcnq1 ICR. More importantly, for the first time, we document that NF-Y is involved in maintaining the antisense promoter activity against strong silencing conditions.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antisense Elements (Genetics)
  • Base Sequence
  • Binding Sites / genetics
  • CCAAT-Binding Factor / chemistry
  • CCAAT-Binding Factor / genetics
  • CCAAT-Binding Factor / metabolism*
  • Cell Line
  • DNA / genetics
  • Epigenesis, Genetic
  • Gene Expression Regulation
  • Gene Silencing
  • Genomic Imprinting
  • Humans
  • KCNQ Potassium Channels
  • KCNQ1 Potassium Channel
  • Membrane Proteins / chemistry
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • Mice
  • Potassium Channels, Voltage-Gated / chemistry
  • Potassium Channels, Voltage-Gated / genetics*
  • Potassium Channels, Voltage-Gated / metabolism
  • Promoter Regions, Genetic
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism
  • Sequence Deletion

Substances

  • Antisense Elements (Genetics)
  • CCAAT-Binding Factor
  • KCNQ Potassium Channels
  • KCNQ1 Potassium Channel
  • KCNQ1 protein, human
  • KCNQ1OT1 long non-coding RNA, human
  • Kcnq1 protein, mouse
  • Membrane Proteins
  • Potassium Channels, Voltage-Gated
  • Recombinant Proteins
  • DNA