Defects in the Alternative Splicing-Dependent Regulation of REST Cause Deafness

Cell. 2018 Jul 26;174(3):536-548.e21. doi: 10.1016/j.cell.2018.06.004. Epub 2018 Jun 28.

Abstract

The DNA-binding protein REST forms complexes with histone deacetylases (HDACs) to repress neuronal genes in non-neuronal cells. In differentiating neurons, REST is downregulated predominantly by transcriptional silencing. Here we report that post-transcriptional inactivation of REST by alternative splicing is required for hearing in humans and mice. We show that, in the mechanosensory hair cells of the mouse ear, regulated alternative splicing of a frameshift-causing exon into the Rest mRNA is essential for the derepression of many neuronal genes. Heterozygous deletion of this alternative exon of mouse Rest causes hair cell degeneration and deafness, and the HDAC inhibitor SAHA (Vorinostat) rescues the hearing of these mice. In humans, inhibition of the frameshifting splicing event by a novel REST variant is associated with dominantly inherited deafness. Our data reveal the necessity for alternative splicing-dependent regulation of REST in hair cells, and they identify a potential treatment for a group of hereditary deafness cases.

Keywords: DFNA27; NRSF; REST; alternative splicing; cochlear hair cells; deafness; gene expression regulation; histone deacetylase inhibitors; inner ear; vestibular hair cells.

Publication types

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

MeSH terms

  • Alternative Splicing / genetics
  • Animals
  • Cell Line
  • Deafness / genetics*
  • Exons
  • Gene Expression Regulation / genetics
  • HEK293 Cells
  • Hair Cells, Auditory / physiology
  • Hearing / genetics
  • Hearing / physiology
  • Histone Deacetylase Inhibitors / metabolism
  • Histone Deacetylases / metabolism
  • Humans
  • Mice
  • Mice, Inbred C57BL
  • Neurons
  • RNA Splicing / genetics
  • Repressor Proteins / genetics*
  • Repressor Proteins / metabolism*
  • Repressor Proteins / physiology
  • Transcription Factors
  • Vorinostat / pharmacology

Substances

  • Histone Deacetylase Inhibitors
  • RE1-silencing transcription factor
  • Repressor Proteins
  • Transcription Factors
  • Vorinostat
  • Histone Deacetylases