Blockade of the PI-3K signalling pathway by the Aggregatibacter actinomycetemcomitans cytolethal distending toxin induces macrophages to synthesize and secrete pro-inflammatory cytokines

Cell Microbiol. 2014 Sep;16(9):1391-404. doi: 10.1111/cmi.12299. Epub 2014 May 1.

Abstract

The Aggregatibactor actinomycetemcomitans cytolethal distending toxin (Cdt) induces G2 arrest and apoptosis in lymphocytes; these toxic effects are due to the active subunit, CdtB, which functions as a phosphatidylinositol-3,4,5-triphosphate (PIP3) phosphatase. We now extend our investigation and demonstrate that Cdt is able to perturb human macrophage function. THP-1- and monocyte-derived macrophages were found not to be susceptible to Cdt-induced apoptosis. Nonetheless, the toxin was capable of binding to macrophages and perturbing PI-3K signalling resulting in decreased PIP3 levels and reduced phosphorylation of Akt and GSK3β; these changes were accompanied by concomitant alterations in kinase activity. Exposure of monocytes and macrophages to Cdt resulted in pro-inflammatory cytokine production including increased expression and release of IL-1β, TNFα and IL-6. Furthermore, treatment of cells with either TLR-2, -3 or -4 agonists in the presence of Cdt resulted in an augmented pro-inflammatory response relative to agonist alone. GSK3β inhibitors blocked the Cdt-induced pro-inflammatory cytokine response suggesting a pivotal role for PI-3K blockade, concomitant decrease in GSK3β phosphorylation and increased kinase activity. Collectively, these studies provide new insight into the virulence potential of Cdt in mediating the pathogenesis of disease caused by Cdt-producing organisms.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Aggregatibacter actinomycetemcomitans / immunology*
  • Bacterial Toxins / immunology*
  • Cytokines / immunology*
  • Interleukin-1beta / metabolism
  • Interleukin-6 / metabolism
  • Macrophages / immunology*
  • Phosphatidylinositol 3-Kinases / metabolism*
  • Signal Transduction*
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Bacterial Toxins
  • Cytokines
  • Interleukin-1beta
  • Interleukin-6
  • Tumor Necrosis Factor-alpha
  • cytolethal distending toxin