C2H2-zinc-finger transcription factors bind RNA and function in diverse post-transcriptional regulatory processes

Mol Cell. 2024 Oct 3;84(19):3810-3825.e10. doi: 10.1016/j.molcel.2024.08.037. Epub 2024 Sep 19.

Abstract

Cys2-His2 zinc-finger proteins (C2H2-ZNFs) constitute the largest class of DNA-binding transcription factors (TFs) yet remain largely uncharacterized. Although certain family members, e.g., GTF3A, have been shown to bind both DNA and RNA, the extent to which C2H2-ZNFs interact with-and regulate-RNA-associated processes is not known. Using UV crosslinking and immunoprecipitation (CLIP), we observe that 148 of 150 analyzed C2H2-ZNFs bind directly to RNA in human cells. By integrating CLIP sequencing (CLIP-seq) RNA-binding maps for 50 of these C2H2-ZNFs with data from chromatin immunoprecipitation sequencing (ChIP-seq), protein-protein interaction assays, and transcriptome profiling experiments, we observe that the RNA-binding profiles of C2H2-ZNFs are generally distinct from their DNA-binding preferences and that they regulate a variety of post-transcriptional processes, including pre-mRNA splicing, cleavage and polyadenylation, and m6A modification of mRNA. Our results thus define a substantially expanded repertoire of C2H2-ZNFs that bind RNA and provide an important resource for elucidating post-transcriptional regulatory programs.

Keywords: C2H2-ZNFs; ChIP-seq; RBPs; RNA-binding; alternative splicing; iCLIP-seq; m6A; mRNA modification; proteomics.

MeSH terms

  • Binding Sites
  • CYS2-HIS2 Zinc Fingers / genetics
  • Chromatin Immunoprecipitation Sequencing
  • Gene Expression Regulation
  • HEK293 Cells
  • Humans
  • Polyadenylation
  • Protein Binding*
  • RNA / genetics
  • RNA / metabolism
  • RNA Processing, Post-Transcriptional
  • RNA Splicing
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • RNA-Binding Proteins / genetics
  • RNA-Binding Proteins / metabolism
  • Transcription Factors* / genetics
  • Transcription Factors* / metabolism

Substances

  • Transcription Factors
  • RNA
  • RNA, Messenger
  • RNA-Binding Proteins