Pneumococcal sialidase promotes bacterial survival by fine-tuning of pneumolysin-mediated membrane disruption

Cell Rep. 2024 Mar 26;43(3):113962. doi: 10.1016/j.celrep.2024.113962. Epub 2024 Mar 13.

Abstract

Pneumolysin (Ply) is an indispensable cholesterol-dependent cytolysin for pneumococcal infection. Although Ply-induced disruption of pneumococci-containing endosomal vesicles is a prerequisite for the evasion of endolysosomal bacterial clearance, its potent activity can be a double-edged sword, having a detrimental effect on bacterial survivability by inducing severe endosomal disruption, bactericidal autophagy, and scaffold epithelial cell death. Thus, Ply activity must be maintained at optimal levels. We develop a highly sensitive assay to monitor endosomal disruption using NanoBiT-Nanobody, which shows that the pneumococcal sialidase NanA can fine-tune Ply activity by trimming sialic acid from cell-membrane-bound glycans. In addition, oseltamivir, an influenza A virus sialidase inhibitor, promotes Ply-induced endosomal disruption and cytotoxicity by inhibiting NanA activity in vitro and greater tissue damage and bacterial clearance in vivo. Our findings provide a foundation for innovative therapeutic strategies for severe pneumococcal infections by exploiting the duality of Ply activity.

Keywords: CP: Cell biology; CP: Microbiology; NanA; NanoBiT; Streptococcus pneumoinae; cytotoxicity; endosome disrupture; nanobody; oseltamivir; pneumolysin; sialic acid; xenophagy.

MeSH terms

  • Bacterial Proteins / metabolism
  • Humans
  • Neuraminidase* / metabolism
  • Pneumococcal Infections*
  • Streptococcus pneumoniae / metabolism
  • Streptolysins / metabolism

Substances

  • plY protein, Streptococcus pneumoniae
  • Neuraminidase
  • Streptolysins
  • Bacterial Proteins