Phosphoribosyl-linked serine ubiquitination of USP14 by the SidE family effectors of Legionella excludes p62 from the bacterial phagosome

Cell Rep. 2023 Aug 29;42(8):112817. doi: 10.1016/j.celrep.2023.112817. Epub 2023 Jul 19.

Abstract

Xenophagy is an evolutionarily conserved host defensive mechanism to eliminate invading microorganisms through autophagic machinery. The intracellular bacterial pathogen Legionella pneumophila can avoid clearance by the xenophagy pathway via the actions of multiple Dot/Icm effector proteins. Previous studies have shown that p62, an adaptor protein involved in xenophagy signaling, is excluded from Legionella-containing vacuoles (LCVs). Such defects are attributed to the multifunctional SidE family effectors (SidEs) that exhibit classic deubiquitinase (DUB) and phosphoribosyl ubiquitination (PR-ubiquitination) activities, yet the mechanism remains elusive. In the present study, we demonstrate that the host DUB USP14 is PR-ubiquitinated by SidEs at multiple serine residues, which impairs its DUB activity and its interactions with p62. The exclusion of p62 from the bacterial phagosome requires the ubiquitin ligase but not the DUB activity of SidEs. These results reveal that PR-ubiquitination of USP14 by SidEs contributes to the evasion of xenophagic clearance by L. pneumophila.

Keywords: CP: Microbiology; Legionella; SdeA; SidEs; USP14; autophagy; effector proteins; p62; phosphoribosyl-linked serine ubiquitination; type IV secretion system; xenophagy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacterial Proteins / metabolism
  • Humans
  • Legionella* / metabolism
  • Legionnaires' Disease* / metabolism
  • Phagosomes / metabolism
  • Serine / metabolism
  • Ubiquitin / metabolism
  • Ubiquitin Thiolesterase / metabolism
  • Ubiquitination
  • Vacuoles / metabolism

Substances

  • Serine
  • Bacterial Proteins
  • Ubiquitin
  • USP14 protein, human
  • Ubiquitin Thiolesterase