A short SUMOylation tag modulates transcription factor activity

J Biol Chem. 2025 Nov;301(11):110807. doi: 10.1016/j.jbc.2025.110807. Epub 2025 Oct 8.

Abstract

SUMOylation is a posttranslational modification that regulates multiple aspects of protein biology, including the activity of transcription factors such as p53. Although strategies exist to decrease protein SUMOylation in a targeted manner, options are limited to increase SUMOylation in a protein-specific manner. Here, we developed a strategy to induce SUMOylation of a target protein relying on its genetic fusion to a 32-residue tag termed ZNF and composed of the SUMO E3 module of ZNF451. Through in vitro and cell-based assays, we establish that this SUMOylation tag promotes robust poly/multi-SUMOylation of p53, used as a model substrate, with a strong preference for SUMO2/3 as compared to SUMO1. Mass spectrometry experiments performed on transfected HEK293 cells stably expressing a modified form of SUMO3 indicate that lysine 386, the main SUMOylation acceptor site of p53, is the primary target of ZNF-mediated SUMOylation. Increased SUMOylation represses p53 transcriptional activity in luciferase reporter assays, a result compatible with the general repressive effects of SUMOylation on transcription factor activity. Finally, fusion of ZNF to HSF1 and DNMT3A also increase their SUMOylation level, showcasing that ZNF could potentially be used to promote the SUMOylation of a broad range of proteins implicated in DNA metabolism. Overall, this strategy will facilitate the investigation of the impact of increased SUMOylation on specific protein substrates.

Keywords: SUMO E3 ligase; SUMOylation; SUMOylation tag; ZNF451; p53; small ubiquitin-like modifier (SUMO); transcription factor.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • DNA Methyltransferase 3A
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • HEK293 Cells
  • Heat Shock Transcription Factors / metabolism
  • Humans
  • Small Ubiquitin-Related Modifier Proteins* / genetics
  • Small Ubiquitin-Related Modifier Proteins* / metabolism
  • Sumoylation*
  • Transcription Factors* / genetics
  • Transcription Factors* / metabolism
  • Tumor Suppressor Protein p53* / genetics
  • Tumor Suppressor Protein p53* / metabolism
  • Ubiquitins

Substances

  • Transcription Factors
  • Tumor Suppressor Protein p53
  • DNA-Binding Proteins
  • DNA Methyltransferase 3A
  • Heat Shock Transcription Factors
  • DNMT3A protein, human
  • HSF1 protein, human
  • Small Ubiquitin-Related Modifier Proteins
  • TP53 protein, human
  • SUMO3 protein, human
  • Ubiquitins