Loss of Kdm5c Causes Spurious Transcription and Prevents the Fine-Tuning of Activity-Regulated Enhancers in Neurons

Cell Rep. 2017 Oct 3;21(1):47-59. doi: 10.1016/j.celrep.2017.09.014.

Abstract

During development, chromatin-modifying enzymes regulate both the timely establishment of cell-type-specific gene programs and the coordinated repression of alternative cell fates. To dissect the role of one such enzyme, the intellectual-disability-linked lysine demethylase 5C (Kdm5c), in the developing and adult brain, we conducted parallel behavioral, transcriptomic, and epigenomic studies in Kdm5c-null and forebrain-restricted inducible knockout mice. Together, genomic analyses and functional assays demonstrate that Kdm5c plays a critical role as a repressor responsible for the developmental silencing of germline genes during cellular differentiation and in fine-tuning activity-regulated enhancers during neuronal maturation. Although the importance of these functions declines after birth, Kdm5c retains an important genome surveillance role preventing the incorrect activation of non-neuronal and cryptic promoters in adult neurons.

Keywords: Claes-Jensen syndrome; DNA methylation; enhancer; epigenetic repression; germline gene silencing; histone methylation; immediate early gene; intellectual disability; lysine demethylase 5C; spurious transcription.

MeSH terms

  • Animals
  • DNA-Binding Proteins
  • Doublecortin Domain Proteins
  • Enhancer Elements, Genetic
  • Female
  • Gene Expression Regulation, Developmental*
  • Glial Fibrillary Acidic Protein / genetics
  • Glial Fibrillary Acidic Protein / metabolism
  • Histone Demethylases
  • Histones / genetics
  • Histones / metabolism
  • Male
  • Maze Learning
  • Mice
  • Mice, Knockout
  • Microtubule-Associated Proteins / genetics
  • Microtubule-Associated Proteins / metabolism
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism
  • Neurons / metabolism*
  • Neurons / pathology
  • Neuropeptides / genetics
  • Neuropeptides / metabolism
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism
  • Oxidoreductases, N-Demethylating / deficiency
  • Oxidoreductases, N-Demethylating / genetics*
  • Prosencephalon / metabolism*
  • Prosencephalon / pathology
  • Signal Transduction
  • Transcription, Genetic*

Substances

  • DNA-Binding Proteins
  • Doublecortin Domain Proteins
  • Glial Fibrillary Acidic Protein
  • Histones
  • Microtubule-Associated Proteins
  • Mtap2 protein, mouse
  • Nerve Tissue Proteins
  • NeuN protein, mouse
  • Neuropeptides
  • Nuclear Proteins
  • glial fibrillary astrocytic protein, mouse
  • Histone Demethylases
  • Kdm5c protein, mouse
  • Oxidoreductases, N-Demethylating