Senataxin Mutation Reveals How R-Loops Promote Transcription by Blocking DNA Methylation at Gene Promoters

Mol Cell. 2018 Feb 1;69(3):426-437.e7. doi: 10.1016/j.molcel.2017.12.030. Epub 2018 Jan 27.

Abstract

R-loops are three-stranded nucleic acid structures found abundantly and yet often viewed as by-products of transcription. Studying cells from patients with a motor neuron disease (amyotrophic lateral sclerosis 4 [ALS4]) caused by a mutation in senataxin, we uncovered how R-loops promote transcription. In ALS4 patients, the senataxin mutation depletes R-loops with a consequent effect on gene expression. With fewer R-loops in ALS4 cells, the expression of BAMBI, a negative regulator of transforming growth factor β (TGF-β), is reduced; that then leads to the activation of the TGF-β pathway. We uncovered that genome-wide R-loops influence promoter methylation of over 1,200 human genes. DNA methyl-transferase 1 favors binding to double-stranded DNA over R-loops. Thus, in forming R-loops, nascent RNA blocks DNA methylation and promotes further transcription. Hence, our results show that nucleic acid structures, in addition to sequences, influence the binding and activity of regulatory proteins.

Keywords: ALS; ALS4; DNA methylation; R-loop; TGFB; amyotrophic lateral sclerosis; helicase; motor neuron disease; senataxin; transcription.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amyotrophic Lateral Sclerosis / genetics
  • Amyotrophic Lateral Sclerosis / metabolism
  • DNA (Cytosine-5-)-Methyltransferase 1 / metabolism
  • DNA / genetics
  • DNA / ultrastructure
  • DNA Helicases
  • DNA Methylation / genetics
  • Gene Expression Regulation / genetics*
  • Humans
  • Membrane Proteins / metabolism
  • Multifunctional Enzymes
  • Mutation
  • Promoter Regions, Genetic* / genetics
  • Protein Processing, Post-Translational
  • RNA / genetics
  • RNA / ultrastructure
  • RNA Helicases / genetics*
  • RNA Helicases / metabolism*
  • RNA-Binding Motifs
  • Transcriptional Activation / genetics
  • Transforming Growth Factor beta / metabolism

Substances

  • BAMBI protein, human
  • Membrane Proteins
  • Multifunctional Enzymes
  • Transforming Growth Factor beta
  • RNA
  • DNA
  • DNA (Cytosine-5-)-Methyltransferase 1
  • DNMT1 protein, human
  • SETX protein, human
  • DNA Helicases
  • RNA Helicases