The X-linked mental retardation gene SMCX/JARID1C defines a family of histone H3 lysine 4 demethylases

Cell. 2007 Mar 23;128(6):1077-88. doi: 10.1016/j.cell.2007.02.017. Epub 2007 Feb 22.

Abstract

Histone methylation regulates chromatin structure and transcription. The recently identified histone demethylase lysine-specific demethylase 1 (LSD1) is chemically restricted to demethylation of only mono- and di- but not trimethylated histone H3 lysine 4 (H3K4me3). We show that the X-linked mental retardation (XLMR) gene SMCX (JARID1C), which encodes a JmjC-domain protein, reversed H3K4me3 to di- and mono- but not unmethylated products. Other SMCX family members, including SMCY, RBP2, and PLU-1, also demethylated H3K4me3. SMCX bound H3K9me3 via its N-terminal PHD (plant homeodomain) finger, which may help coordinate H3K4 demethylation and H3K9 methylation in transcriptional repression. Significantly, several XLMR-patient point mutations reduced SMCX demethylase activity and binding to H3K9me3 peptides, respectively. Importantly, studies in zebrafish and primary mammalian neurons demonstrated a role for SMCX in neuronal survival and dendritic development and a link to the demethylase activity. Our findings thus identify a family of H3K4me3 demethylases and uncover a critical link between histone modifications and XLMR.

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

  • Animals
  • Cell Line, Tumor
  • Cell Survival
  • DNA, Complementary
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Gene Library
  • Histone Demethylases
  • Histone-Lysine N-Methyltransferase / genetics
  • Histone-Lysine N-Methyltransferase / metabolism
  • Histones / chemistry
  • Histones / metabolism*
  • Humans
  • Intracellular Signaling Peptides and Proteins / genetics
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Jumonji Domain-Containing Histone Demethylases
  • Lysine / metabolism
  • Mental Retardation, X-Linked / genetics*
  • Methylation
  • Mice
  • Minor Histocompatibility Antigens
  • Neoplasm Proteins / genetics
  • Neoplasm Proteins / metabolism
  • Neurons / cytology
  • Neurons / metabolism
  • Oxidoreductases, N-Demethylating / genetics*
  • Oxidoreductases, N-Demethylating / metabolism
  • Proteins / genetics*
  • Proteins / metabolism
  • Retinoblastoma-Binding Protein 2
  • Tumor Suppressor Proteins / genetics
  • Tumor Suppressor Proteins / metabolism

Substances

  • DNA, Complementary
  • DNA-Binding Proteins
  • Histones
  • Intracellular Signaling Peptides and Proteins
  • Minor Histocompatibility Antigens
  • Neoplasm Proteins
  • Proteins
  • Tumor Suppressor Proteins
  • Histone Demethylases
  • Jumonji Domain-Containing Histone Demethylases
  • KDM5A protein, human
  • KDM5C protein, human
  • KDM5D protein, human
  • Kdm5b protein, mouse
  • Retinoblastoma-Binding Protein 2
  • Oxidoreductases, N-Demethylating
  • Histone-Lysine N-Methyltransferase
  • Lysine