A specific LSD1/KDM1A isoform regulates neuronal differentiation through H3K9 demethylation

Mol Cell. 2015 Mar 19;57(6):957-970. doi: 10.1016/j.molcel.2015.01.010. Epub 2015 Feb 12.

Abstract

Lysine-specific demethylase 1 (LSD1) has been reported to repress and activate transcription by mediating histone H3K4me1/2 and H3K9me1/2 demethylation, respectively. The molecular mechanism that underlies this dual substrate specificity has remained unknown. Here we report that an isoform of LSD1, LSD1+8a, does not have the intrinsic capability to demethylate H3K4me2. Instead, LSD1+8a mediates H3K9me2 demethylation in collaboration with supervillin (SVIL), a new LSD1+8a interacting protein. LSD1+8a knockdown increases H3K9me2, but not H3K4me2, levels at its target promoters and compromises neuronal differentiation. Importantly, SVIL co-localizes to LSD1+8a-bound promoters, and its knockdown mimics the impact of LSD1+8a loss, supporting SVIL as a cofactor for LSD1+8a in neuronal cells. These findings provide insight into mechanisms by which LSD1 mediates H3K9me demethylation and highlight alternative splicing as a means by which LSD1 acquires selective substrate specificities (H3K9 versus H3K4) to differentially control specific gene expression programs in neurons.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Alternative Splicing
  • Cell Differentiation
  • Cell Movement
  • Gene Expression Regulation
  • Gene Knockdown Techniques
  • HeLa Cells
  • Histone Demethylases / genetics
  • Histone Demethylases / metabolism*
  • Histones / genetics
  • Histones / metabolism
  • Humans
  • Lysine / metabolism
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism*
  • Methylation
  • Microfilament Proteins / genetics
  • Microfilament Proteins / metabolism*
  • Neurons / cytology
  • Neurons / metabolism*
  • Promoter Regions, Genetic
  • Protein Isoforms / metabolism

Substances

  • Histones
  • Membrane Proteins
  • Microfilament Proteins
  • Protein Isoforms
  • SVIL protein, human
  • Histone Demethylases
  • KDM1A protein, human
  • Lysine