Specific catalytically impaired DDX3X mutants form sexually dimorphic hollow condensates

Nat Commun. 2024 Nov 5;15(1):9553. doi: 10.1038/s41467-024-53636-0.

Abstract

Mutations in the RNA helicase DDX3X, implicated in various cancers and neurodevelopmental disorders, often impair RNA unwinding and translation. However, the mechanisms underlying the impairment and the differential interactions of DDX3X mutants with wild-type (WT) X-linked DDX3X and Y-linked homolog DDX3Y remain elusive. This study reveals that specific DDX3X mutants more frequently found in disease form distinct hollow condensates in cells. Using a combined structural, biochemical, and single-molecule microscopy study, we show that reduced ATPase and RNA release activities contribute to condensate formation and these catalytic deficits result from inhibiting the catalytic cycle at multiple steps. Proteomic investigations further demonstrate that these hollow condensates sequester WT DDX3X/DDX3Y and other proteins crucial for diverse signaling pathways. WT DDX3X enhances the dynamics of heterogeneous mutant/WT hollow condensates more effectively than DDX3Y. These findings offer valuable insights into the catalytic defects of specific DDX3X mutants and their differential interactions with wild-type DDX3X and DDX3Y, potentially explaining sex biases in disease.

MeSH terms

  • Adenosine Triphosphatases / genetics
  • Adenosine Triphosphatases / metabolism
  • Animals
  • Catalysis
  • DEAD-box RNA Helicases* / genetics
  • DEAD-box RNA Helicases* / metabolism
  • Female
  • HEK293 Cells
  • Humans
  • Male
  • Minor Histocompatibility Antigens
  • Mutation*
  • Proteomics / methods
  • RNA / genetics
  • RNA / metabolism
  • Single Molecule Imaging

Substances

  • DEAD-box RNA Helicases
  • DDX3X protein, human
  • RNA
  • DDX3Y protein, human
  • Adenosine Triphosphatases
  • Minor Histocompatibility Antigens