Toxoplasma gondii UBL-UBA shuttle proteins contribute to the degradation of ubiquitinylated proteins and are important for synchronous cell division and virulence

FASEB J. 2020 Oct;34(10):13711-13725. doi: 10.1096/fj.202000759RR. Epub 2020 Aug 17.

Abstract

Toxoplasma gondii is an obligate intracellular apicomplexan parasite that causes lethal diseases in immunocompromised patients. Ubiquitin-proteasome system (UPS) regulates many cellular processes by degrading ubiquitinylated proteins. The UBL-UBA shuttle protein family, which escorts the ubiquitinylated proteins to the proteasome for degradation, are crucial components of UPS. Here, we identified three UBL-UBA shuttle proteins (TGGT1_304680, DNA damage inducible protein 1, DDI1; TGGT1_295340, UV excision repair protein rad23 protein, RAD23; and TGGT1_223680, ubiquitin family protein, DSK2) localized in the cytoplasm and nucleus of T gondii. Deletion of shuttle proteins inhibited parasites growth and resulted in accumulation of ubiquitinylated proteins. Cell division of triple-gene knockout strain was asynchronous. In addition, we found that the retroviral aspartic protease activity of the nonclassical shuttle protein DDI1 was important for the virulence of Toxoplasma in mice. These results showed the critical roles of UBL-UBA shuttle proteins in regulating the degradation of ubiquitinylated proteins and cell division of T gondii.

Keywords: Toxoplasma gondii; UBL-UBA shuttle protein family; cell division; degradation of ubiquitinylated proteins; retroviral aspartic protease activity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Division*
  • Cell Line
  • Female
  • Humans
  • Mice
  • Mice, Inbred BALB C
  • Proteasome Endopeptidase Complex / metabolism*
  • Proteolysis
  • Protozoan Proteins / genetics
  • Protozoan Proteins / metabolism*
  • Toxoplasma / metabolism*
  • Toxoplasma / pathogenicity
  • Ubiquitination
  • Ubiquitins / genetics
  • Ubiquitins / metabolism*
  • Virulence / genetics

Substances

  • Protozoan Proteins
  • Ubiquitins
  • Proteasome Endopeptidase Complex