Ubiquitination independent of E1 and E2 enzymes by bacterial effectors

Nature. 2016 May 5;533(7601):120-4. doi: 10.1038/nature17657. Epub 2016 Apr 6.

Abstract

Signalling by ubiquitination regulates virtually every cellular process in eukaryotes. Covalent attachment of ubiquitin to a substrate is catalysed by the E1, E2 and E3 three-enzyme cascade, which links the carboxy terminus of ubiquitin to the ε-amino group of, in most cases, a lysine of the substrate via an isopeptide bond. Given the essential roles of ubiquitination in the regulation of the immune system, it is not surprising that the ubiquitination network is a common target for diverse infectious agents. For example, many bacterial pathogens exploit ubiquitin signalling using virulence factors that function as E3 ligases, deubiquitinases or as enzymes that directly attack ubiquitin. The bacterial pathogen Legionella pneumophila utilizes approximately 300 effectors that modulate diverse host processes to create a permissive niche for its replication in phagocytes. Here we demonstrate that members of the SidE effector family of L. pneumophila ubiquitinate multiple Rab small GTPases associated with the endoplasmic reticulum. Moreover, we show that these proteins are capable of catalysing ubiquitination without the need for the E1 and E2 enzymes. A putative mono-ADP-ribosyltransferase motif critical for the ubiquitination activity is also essential for the role of the SidE family in intracellular bacterial replication in a protozoan host. The E1/E2-independent ubiquitination catalysed by these enzymes is energized by nicotinamide adenine dinucleotide, which activates ubiquitin by the formation of ADP-ribosylated ubiquitin. These results establish that ubiquitination can be catalysed by a single enzyme, the activity of which does not require ATP.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • ADP Ribose Transferases / chemistry
  • ADP Ribose Transferases / metabolism
  • Adenosine Diphosphate Ribose / metabolism
  • Adenosine Triphosphate
  • Amino Acid Motifs
  • Amino Acid Sequence
  • Bacterial Load
  • Bacterial Proteins / metabolism*
  • Biocatalysis
  • Endoplasmic Reticulum / enzymology
  • Endoplasmic Reticulum / metabolism
  • Legionella pneumophila / chemistry*
  • Legionella pneumophila / cytology
  • Legionella pneumophila / enzymology
  • Legionella pneumophila / pathogenicity
  • Membrane Proteins / metabolism
  • Molecular Sequence Data
  • NAD / metabolism
  • Ubiquitin / chemistry
  • Ubiquitin / metabolism
  • Ubiquitin-Activating Enzymes
  • Ubiquitin-Conjugating Enzymes
  • Ubiquitination*
  • Virulence Factors / metabolism
  • rab GTP-Binding Proteins / chemistry
  • rab GTP-Binding Proteins / metabolism

Substances

  • Bacterial Proteins
  • Membrane Proteins
  • SdeA protein, Legionella pneumophila
  • Ubiquitin
  • Virulence Factors
  • NAD
  • Adenosine Diphosphate Ribose
  • Adenosine Triphosphate
  • Ubiquitin-Conjugating Enzymes
  • ADP Ribose Transferases
  • rab GTP-Binding Proteins
  • Ubiquitin-Activating Enzymes