ncRNA- and Pc2 methylation-dependent gene relocation between nuclear structures mediates gene activation programs

Cell. 2011 Nov 11;147(4):773-88. doi: 10.1016/j.cell.2011.08.054.

Abstract

Although eukaryotic nuclei contain distinct architectural structures associated with noncoding RNAs (ncRNAs), their potential relationship to regulated transcriptional programs remains poorly understood. Here, we report that methylation/demethylation of Polycomb 2 protein (Pc2) controls relocation of growth-control genes between Polycomb bodies (PcGs) and interchromatin granules (ICGs) in response to growth signals. This movement is the consequence of binding of methylated and unmethylated Pc2 to the ncRNAs TUG1 and MALAT1/NEAT2, located in PcGs and ICGs, respectively. These ncRNAs mediate assembly of multiple corepressors/coactivators and can serve to switch mark recognition by "readers" of the histone code. Additionally, binding of NEAT2 to unmethylated Pc2 promotes E2F1 SUMOylation, leading to activation of the growth-control gene program. These observations delineate a molecular pathway linking the actions of subnuclear structure-specific ncRNAs and nonhistone protein methylation to relocation of transcription units in the three-dimensional space of the nucleus, thus achieving coordinated gene expression programs.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Amino Acid Sequence
  • Cell Line
  • Cell Nucleus / metabolism*
  • Chromatin / metabolism
  • E2F1 Transcription Factor / metabolism
  • Gene Expression Regulation*
  • HeLa Cells
  • Humans
  • Ligases
  • Methylation
  • Methyltransferases / metabolism
  • Molecular Sequence Data
  • Polycomb-Group Proteins
  • RNA, Long Noncoding
  • RNA, Untranslated / metabolism*
  • Repressor Proteins / chemistry
  • Repressor Proteins / metabolism*
  • Sumoylation
  • Transcription, Genetic
  • Ubiquitin-Protein Ligases
  • Ubiquitination

Substances

  • CDCA7L protein, human
  • Chromatin
  • E2F1 Transcription Factor
  • E2F1 protein, human
  • MALAT1 long non-coding RNA, human
  • Polycomb-Group Proteins
  • RNA, Long Noncoding
  • RNA, Untranslated
  • Repressor Proteins
  • SUV39H1 protein, human
  • Methyltransferases
  • Ubiquitin-Protein Ligases
  • Ligases
  • CBX4 protein, human