A role for the Cockayne Syndrome B (CSB)-Elongin ubiquitin ligase complex in signal-dependent RNA polymerase II transcription

J Biol Chem. 2021 Jul;297(1):100862. doi: 10.1016/j.jbc.2021.100862. Epub 2021 Jun 9.

Abstract

The Elongin complex was originally identified as an RNA polymerase II (RNAPII) elongation factor and subsequently as the substrate recognition component of a Cullin-RING E3 ubiquitin ligase. More recent evidence indicates that the Elongin ubiquitin ligase assembles with the Cockayne syndrome B helicase (CSB) in response to DNA damage and can target stalled polymerases for ubiquitylation and removal from the genome. In this report, we present evidence that the CSB-Elongin ubiquitin ligase pathway has roles beyond the DNA damage response in the activation of RNAPII-mediated transcription. We observed that assembly of the CSB-Elongin ubiquitin ligase is induced not just by DNA damage, but also by a variety of signals that activate RNAPII-mediated transcription, including endoplasmic reticulum (ER) stress, amino acid starvation, retinoic acid, glucocorticoids, and doxycycline treatment of cells carrying several copies of a doxycycline-inducible reporter. Using glucocorticoid receptor (GR)-regulated genes as a model, we showed that glucocorticoid-induced transcription is accompanied by rapid recruitment of CSB and the Elongin ubiquitin ligase to target genes in a step that depends upon the presence of transcribing RNAPII on those genes. Consistent with the idea that the CSB-Elongin pathway plays a direct role in GR-regulated transcription, mouse cells lacking the Elongin subunit Elongin A exhibit delays in both RNAPII accumulation on and dismissal from target genes following glucocorticoid addition and withdrawal, respectively. Taken together, our findings bring to light a new role for the CSB-Elongin pathway in RNAPII-mediated transcription.

Keywords: Cockayne syndrome B (CSB); Elongin; RNA polymerase II; chromatin immunoprecipitation (ChIP); fluorescence resonance energy transfer (FRET); glucocorticoid receptor; transcription elongation factor; transcription regulation; ubiquitin ligase.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cockayne Syndrome / enzymology
  • Cockayne Syndrome / genetics
  • DNA Helicases / chemistry
  • DNA Helicases / genetics*
  • DNA Helicases / ultrastructure
  • DNA Repair / genetics
  • DNA Repair Enzymes / chemistry
  • DNA Repair Enzymes / genetics*
  • DNA Repair Enzymes / ultrastructure
  • Elongin / chemistry
  • Elongin / genetics*
  • Elongin / ultrastructure
  • Humans
  • Mice
  • Multiprotein Complexes / chemistry
  • Multiprotein Complexes / genetics
  • Multiprotein Complexes / ultrastructure
  • Poly-ADP-Ribose Binding Proteins / chemistry
  • Poly-ADP-Ribose Binding Proteins / genetics*
  • Poly-ADP-Ribose Binding Proteins / ultrastructure
  • RNA Polymerase II / chemistry
  • RNA Polymerase II / genetics*
  • Receptors, Glucocorticoid / chemistry
  • Receptors, Glucocorticoid / genetics
  • Ubiquitin / chemistry
  • Ubiquitin / genetics
  • Ubiquitin-Protein Ligases / chemistry
  • Ubiquitin-Protein Ligases / genetics*
  • Ubiquitin-Protein Ligases / ultrastructure
  • Ubiquitination / genetics

Substances

  • Elongin
  • Multiprotein Complexes
  • Poly-ADP-Ribose Binding Proteins
  • Receptors, Glucocorticoid
  • Ubiquitin
  • CULL-RING ligase, human
  • Ubiquitin-Protein Ligases
  • RNA Polymerase II
  • DNA Helicases
  • ERCC6 protein, human
  • DNA Repair Enzymes