Autoinhibition Mechanism of the Ubiquitin-Conjugating Enzyme UBE2S by Autoubiquitination

Structure. 2019 Aug 6;27(8):1195-1210.e7. doi: 10.1016/j.str.2019.05.008. Epub 2019 Jun 20.

Abstract

Ubiquitin-conjugating enzymes (E2s) govern key aspects of ubiquitin signaling. Emerging evidence suggests that the activities of E2s are modulated by posttranslational modifications; the structural underpinnings, however, are largely unclear. Here, we unravel the structural basis and mechanistic consequences of a conserved autoubiquitination event near the catalytic center of E2s, using the human anaphase-promoting complex/cyclosome-associated UBE2S as a model system. Crystal structures we determined of the catalytic ubiquitin carrier protein domain combined with MD simulations reveal that the active-site region is malleable, which permits an adjacent ubiquitin acceptor site, Lys+5, to be ubiquitinated intramolecularly. We demonstrate by NMR that the Lys+5-linked ubiquitin inhibits UBE2S by obstructing its reloading with ubiquitin. By immunoprecipitation, quantitative mass spectrometry, and siRNA-and-rescue experiments we show that Lys+5 ubiquitination of UBE2S decreases during mitotic exit but does not influence proteasomal turnover of this E2. These findings suggest that UBE2S activity underlies inherent regulation during the cell cycle.

Keywords: E2 enzyme; K11 chain; NMR; X-ray crystallography; cell cycle; enzyme mechanism; mass spectrometry; mitosis; molecular dynamics; ubiquitin.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Catalytic Domain
  • Cell Line
  • Crystallography, X-Ray
  • Cysteine / metabolism
  • Gene Expression Regulation
  • HeLa Cells
  • Homeostasis
  • Humans
  • Lysine / metabolism*
  • Mitosis
  • Molecular Dynamics Simulation
  • Ubiquitin / metabolism*
  • Ubiquitin-Conjugating Enzymes / chemistry*
  • Ubiquitin-Conjugating Enzymes / metabolism*
  • Ubiquitination

Substances

  • Ubiquitin
  • Ube2S protein, human
  • Ubiquitin-Conjugating Enzymes
  • Lysine
  • Cysteine