Cockayne syndrome B protein acts as an ATP-dependent processivity factor that helps RNA polymerase II overcome nucleosome barriers

Proc Natl Acad Sci U S A. 2020 Oct 13;117(41):25486-25493. doi: 10.1073/pnas.2013379117. Epub 2020 Sep 28.

Abstract

While loss-of-function mutations in Cockayne syndrome group B protein (CSB) cause neurological diseases, this unique member of the SWI2/SNF2 family of chromatin remodelers has been broadly implicated in transcription elongation and transcription-coupled DNA damage repair, yet its mechanism remains largely elusive. Here, we use a reconstituted in vitro transcription system with purified polymerase II (Pol II) and Rad26, a yeast ortholog of CSB, to study the role of CSB in transcription elongation through nucleosome barriers. We show that CSB forms a stable complex with Pol II and acts as an ATP-dependent processivity factor that helps Pol II across a nucleosome barrier. This noncanonical mechanism is distinct from the canonical modes of chromatin remodelers that directly engage and remodel nucleosomes or transcription elongation factors that facilitate Pol II nucleosome bypass without hydrolyzing ATP. We propose a model where CSB facilitates gene expression by helping Pol II bypass chromatin obstacles while maintaining their structures.

Keywords: Cockayne syndrome; RNA polymerase II; chromatin remodeling; nucleosome bypass; transcription elongation.

Publication types

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

MeSH terms

  • Adenosine Triphosphatases / genetics
  • Adenosine Triphosphatases / metabolism
  • Adenosine Triphosphate / metabolism*
  • DNA Helicases / genetics
  • DNA Helicases / metabolism*
  • DNA Repair Enzymes / genetics
  • DNA Repair Enzymes / metabolism*
  • DNA, Fungal
  • Escherichia coli
  • Gene Expression Regulation, Enzymologic
  • Gene Expression Regulation, Fungal
  • Models, Molecular
  • Mutation
  • Nucleosomes / metabolism*
  • Poly-ADP-Ribose Binding Proteins / genetics
  • Poly-ADP-Ribose Binding Proteins / metabolism*
  • Protein Conformation
  • RNA Polymerase II / genetics
  • RNA Polymerase II / metabolism*
  • Saccharomyces cerevisiae Proteins / genetics
  • Saccharomyces cerevisiae Proteins / metabolism
  • Schizosaccharomyces / metabolism

Substances

  • DNA, Fungal
  • Nucleosomes
  • Poly-ADP-Ribose Binding Proteins
  • Saccharomyces cerevisiae Proteins
  • Adenosine Triphosphate
  • RNA Polymerase II
  • Adenosine Triphosphatases
  • RAD26 protein, S cerevisiae
  • DNA Helicases
  • ERCC6 protein, human
  • DNA Repair Enzymes