Clostridium difficile Toxin A Undergoes Clathrin-Independent, PACSIN2-Dependent Endocytosis

PLoS Pathog. 2016 Dec 12;12(12):e1006070. doi: 10.1371/journal.ppat.1006070. eCollection 2016 Dec.

Abstract

Clostridium difficile infection affects a significant number of hospitalized patients in the United States. Two homologous exotoxins, TcdA and TcdB, are the major virulence factors in C. difficile pathogenesis. The toxins are glucosyltransferases that inactivate Rho family-GTPases to disrupt host cellular function and cause fluid secretion, inflammation, and cell death. Toxicity depends on receptor binding and subsequent endocytosis. TcdB has been shown to enter cells by clathrin-dependent endocytosis, but the mechanism of TcdA uptake is still unclear. Here, we utilize a combination of RNAi-based knockdown, pharmacological inhibition, and cell imaging approaches to investigate the endocytic mechanism(s) that contribute to TcdA uptake and subsequent cytopathic and cytotoxic effects. We show that TcdA uptake and cellular intoxication is dynamin-dependent but does not involve clathrin- or caveolae-mediated endocytosis. Confocal microscopy using fluorescently labeled TcdA shows significant colocalization of the toxin with PACSIN2-positive structures in cells during entry. Disruption of PACSIN2 function by RNAi-based knockdown approaches inhibits TcdA uptake and toxin-induced downstream effects in cells indicating that TcdA entry is PACSIN2-dependent. We conclude that TcdA and TcdB utilize distinct endocytic mechanisms to intoxicate host cells.

MeSH terms

  • Adaptor Proteins, Signal Transducing / metabolism*
  • Animals
  • Bacterial Toxins / metabolism*
  • Blotting, Western
  • Caco-2 Cells
  • Clathrin
  • Clostridioides difficile
  • Clostridium Infections / metabolism*
  • Endocytosis / physiology*
  • Enterotoxins / metabolism*
  • Fluorescent Antibody Technique
  • Gene Knockdown Techniques
  • HEK293 Cells
  • Humans
  • Image Processing, Computer-Assisted
  • Mice
  • Microscopy, Confocal
  • Protein Transport / physiology
  • Reverse Transcriptase Polymerase Chain Reaction
  • Transfection
  • Virulence Factors / metabolism

Substances

  • Adaptor Proteins, Signal Transducing
  • Bacterial Toxins
  • Clathrin
  • Enterotoxins
  • PACSIN2 protein, human
  • Virulence Factors
  • tcdA protein, Clostridium difficile