Gamma interferon-dependent transcriptional memory via relocalization of a gene locus to PML nuclear bodies

Mol Cell Biol. 2010 Apr;30(8):2046-56. doi: 10.1128/MCB.00906-09. Epub 2010 Feb 1.

Abstract

Memory of past cellular responses is an essential adaptation to repeating environmental stimuli. We addressed the question of whether gamma interferon (IFN-gamma)-inducible transcription generates memory that sensitizes cells to a second stimulus. We have found that the major histocompatibility complex class II gene DRA is relocated to promyelocytic leukemia (PML) nuclear bodies upon induction with IFN-gamma, and this topology is maintained long after transcription shut off. Concurrent interaction of PML protein with mixed-lineage leukemia generates a prolonged permissive chromatin state on the DRA gene characterized by high promoter histone H3 K4 dimethylation that facilitates rapid expression upon restimulation. We propose that the primary signal-induced transcription generates spatial and epigenetic memory that is maintained through several cell generations and endows the cell with increased responsiveness to future activation signals.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Chromatin / genetics
  • Chromatin / metabolism
  • Epigenesis, Genetic
  • Genes, MHC Class II*
  • HeLa Cells
  • Histones / genetics
  • Histones / metabolism
  • Humans
  • Interferon-gamma / genetics
  • Interferon-gamma / metabolism*
  • Intranuclear Inclusion Bodies / genetics*
  • Intranuclear Inclusion Bodies / metabolism
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism*
  • Promoter Regions, Genetic
  • Promyelocytic Leukemia Protein
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*
  • Transcription, Genetic*
  • Transcriptional Activation
  • Tumor Suppressor Proteins / genetics
  • Tumor Suppressor Proteins / metabolism*

Substances

  • Chromatin
  • Histones
  • Nuclear Proteins
  • Promyelocytic Leukemia Protein
  • Transcription Factors
  • Tumor Suppressor Proteins
  • PML protein, human
  • Interferon-gamma