Association with TFIIIC limits MYCN localisation in hubs of active promoters and chromatin accumulation of non-phosphorylated RNA polymerase II

Elife. 2024 Aug 23:13:RP94407. doi: 10.7554/eLife.94407.

Abstract

MYC family oncoproteins regulate the expression of a large number of genes and broadly stimulate elongation by RNA polymerase II (RNAPII). While the factors that control the chromatin association of MYC proteins are well understood, much less is known about how interacting proteins mediate MYC's effects on transcription. Here, we show that TFIIIC, an architectural protein complex that controls the three-dimensional chromatin organisation at its target sites, binds directly to the amino-terminal transcriptional regulatory domain of MYCN. Surprisingly, TFIIIC has no discernible role in MYCN-dependent gene expression and transcription elongation. Instead, MYCN and TFIIIC preferentially bind to promoters with paused RNAPII and globally limit the accumulation of non-phosphorylated RNAPII at promoters. Consistent with its ubiquitous role in transcription, MYCN broadly participates in hubs of active promoters. Depletion of TFIIIC further increases MYCN localisation to these hubs. This increase correlates with a failure of the nuclear exosome and BRCA1, both of which are involved in nascent RNA degradation, to localise to active promoters. Our data suggest that MYCN and TFIIIC exert an censoring function in early transcription that limits promoter accumulation of inactive RNAPII and facilitates promoter-proximal degradation of nascent RNA.

Keywords: MYCN; TFIIIC; cancer biology; chromosomes; gene expression; human; neuroblastoma; nuclear exosome; promoter hub.

MeSH terms

  • Cell Line, Tumor
  • Chromatin* / metabolism
  • Humans
  • N-Myc Proto-Oncogene Protein* / genetics
  • N-Myc Proto-Oncogene Protein* / metabolism
  • Promoter Regions, Genetic*
  • Protein Binding
  • RNA Polymerase II* / genetics
  • RNA Polymerase II* / metabolism
  • Transcription Factors, TFII / genetics
  • Transcription Factors, TFII / metabolism
  • Transcription, Genetic

Substances

  • RNA Polymerase II
  • N-Myc Proto-Oncogene Protein
  • MYCN protein, human
  • Chromatin
  • Transcription Factors, TFII

Associated data

  • GEO/GSE223058
  • GEO/GSE111905
  • GEO/GSE164569