Cell-to-cell communication via gap junctions regulates the airway epithelial host defense. Quorum-sensing (QS) molecules produced by Pseudomonas aeruginosa coordinate the virulence factors expression of this opportunistic pathogen, which infects the lung of patients with altered defense. These bacterial signals may also incidentally modulate airway epithelial cell responses to the pathogen, a process called inter-kingdom signaling.
We investigated whether the P. aeruginosa N-3-oxo-dodecanoyl-L-homoserine lactone (C12) QS molecule interferes with gap junctional intercellular communication (GJIC) of airway epithelial cell. C12 degradation and its effects on cells were monitored in human airway epithelial cell models grown under non-polarized and polarized conditions. Its concentration was further monitored in daily tracheal aspirates of intubated patients colonized by P. aeruginosa.
C12 rapidly altered epithelial integrity (inducing shrinkage and blebbing) and decreased GJIC in non-polarized airway epithelial cells while other quorum-sensing molecules had no effect. C12 also increased [Ca2+]i by promoting calcium release from the ER and calcium influx. The cytotoxic effects of C12 were dependent on [Ca2+]i and could be prevented by inhibitors of Src tyrosine family and Rho-associated protein kinases. In contrast, polarized airway cells grown on Transwell filters were protected from C12. In vivo during colonization of intubated patients, C12 did not accumulate, but paralleled bacterial densities. Interestingly, in vitro C12 degradation, a reaction catalyzed by intracellular paraoxonase 2 (PON2), was impaired in non-polarized cells whereas PON2 expression was increased during epithelial polarization. Finally, in a wound injury model of primary airway epithelial cells grown at the air-liquid interface, repeated exposure of C12impairs airway epithelial cell repair.
The cytotoxicity of C12 on non-polarized epithelial cells, combined with its impaired degradation allowing its accumulation, provide an additional pathogenic mechanism for P. aeruginosa infections. Thus, the results highlight the importance of epithelial barrier integrity and polarization as a defense mechanism enabling C12 degradation.