Dysregulated hemolysin liberates bacterial outer membrane vesicles for cytosolic lipopolysaccharide sensing

S Chen, D Yang, Y Wen, Z Jiang, L Zhang… - PLoS …, 2018 - journals.plos.org
S Chen, D Yang, Y Wen, Z Jiang, L Zhang, J Jiang, Y Chen, T Hu, Q Wang, Y Zhang, Q Liu
PLoS pathogens, 2018journals.plos.org
Inflammatory caspase-11/4/5 recognize cytosolic LPS from invading Gram-negative bacteria
and induce pyroptosis and cytokine release, forming rapid innate antibacterial defenses.
Since extracellular or vacuole-constrained bacteria are thought to rarely access the
cytoplasm, how their LPS are exposed to the cytosolic sensors is a critical event for
pathogen recognition. Hemolysin is a pore-forming bacterial toxin, which was generally
accepted to rupture cell membrane, leading to cell lysis. Whether and how hemolysin …
Inflammatory caspase-11/4/5 recognize cytosolic LPS from invading Gram-negative bacteria and induce pyroptosis and cytokine release, forming rapid innate antibacterial defenses. Since extracellular or vacuole-constrained bacteria are thought to rarely access the cytoplasm, how their LPS are exposed to the cytosolic sensors is a critical event for pathogen recognition. Hemolysin is a pore-forming bacterial toxin, which was generally accepted to rupture cell membrane, leading to cell lysis. Whether and how hemolysin participates in non-canonical inflammasome signaling remains undiscovered. Here, we show that hemolysin-overexpressed enterobacteria triggered significantly increased caspase-4 activation in human intestinal epithelial cell lines. Hemolysin promoted LPS cytosolic delivery from extracellular bacteria through dynamin-dependent endocytosis. Further, we revealed that hemolysin was largely associated with bacterial outer membrane vesicles (OMVs) and induced rupture of OMV-containing vacuoles, subsequently increasing LPS exposure to the cytosolic sensor. Accordingly, overexpression of hemolysin promoted caspase-11 dependent IL-18 secretion and gut inflammation in mice, which was associated with restricting bacterial colonization in vivo. Together, our work reveals a concept that hemolysin promotes noncanonical inflammasome activation via liberating OMVs for cytosolic LPS sensing, which offers insights into innate immune surveillance of dysregulated hemolysin via caspase-11/4 in intestinal antibacterial defenses.
PLOS