PGC-1α senses the CBC of pre-mRNA to dictate the fate of promoter-proximally paused RNAPII

Mol Cell. 2023 Jan 19;83(2):186-202.e11. doi: 10.1016/j.molcel.2022.12.022.

Abstract

PGC-1α is well established as a metazoan transcriptional coactivator of cellular adaptation in response to stress. However, the mechanisms by which PGC-1α activates gene transcription are incompletely understood. Here, we report that PGC-1α serves as a scaffold protein that physically and functionally connects the DNA-binding protein estrogen-related receptor α (ERRα), cap-binding protein 80 (CBP80), and Mediator to overcome promoter-proximal pausing of RNAPII and transcriptionally activate stress-response genes. We show that PGC-1α promotes pausing release in a two-arm mechanism (1) by recruiting the positive transcription elongation factor b (P-TEFb) and (2) by outcompeting the premature transcription termination complex Integrator. Using mice homozygous for five amino acid changes in the CBP80-binding motif (CBM) of PGC-1α that destroy CBM function, we show that efficient differentiation of primary myoblasts to myofibers and timely skeletal muscle regeneration after injury require PGC-1α binding to CBP80. Our findings reveal how PGC-1α activates stress-response gene transcription in a previously unanticipated pre-mRNA quality-control pathway.

Keywords: CBP80; ERRα; Integrator; Mediator; P-TEFb; PGC-1α; cap-binding complex; gene transcription; interferon signaling; myogenesis; pre-mRNP quality control; promoter-proximal pausing; skeletal muscle regeneration.

MeSH terms

  • Animals
  • DNA-Binding Proteins / genetics
  • Mice
  • Muscle, Skeletal / metabolism
  • Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha / genetics
  • Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha / metabolism
  • Promoter Regions, Genetic
  • RNA Cap-Binding Proteins / genetics
  • RNA Polymerase II / metabolism
  • RNA Precursors* / metabolism
  • Transcription Factors* / metabolism
  • Transcription, Genetic

Substances

  • DNA-Binding Proteins
  • Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha
  • RNA Cap-Binding Proteins
  • RNA Polymerase II
  • RNA Precursors
  • Transcription Factors
  • Ppargc1a protein, mouse