Insights into biofilm architecture and maturation enable improved clinical strategies for exopolysaccharide-targeting therapeutics

Cell Chem Biol. 2024 Dec 19;31(12):2096-2111.e7. doi: 10.1016/j.chembiol.2024.11.005. Epub 2024 Dec 4.

Abstract

Polysaccharide intercellular adhesin (PIA), an exopolysaccharide composed of poly-N-acetyl glucosamine (PNAG), is an essential component in many pathogenic biofilms. Partial deacetylation of PNAG is required for biofilm formation, but limited structural knowledge hinders therapeutic development. Employing a new monoclonal antibody (TG10) that selectively binds highly deacetylated PNAG and an antibody (F598) in clinical trials that binds highly acetylated PNAG, we demonstrate that PIA within the biofilm contains distinct regions of highly acetylated and deacetylated exopolysaccharide, contrary to the previous model invoking stochastic deacetylation throughout the biofilm. This discovery led us to hypothesize that targeting both forms of PNAG would enhance efficacy. Remarkably, TG10 and F598 synergistically increased in vitro and in vivo activity, providing 90% survival in a lethal Staphylococcus aureus challenge murine model. Our advanced model deepens the conceptual understanding of PIA architecture and maturation and reveals improved design strategies for PIA-targeting therapeutics, vaccines, and diagnostic agents.

Keywords: F598; PIA; PNAG; SPRi array; Staphylococcal infections; TG10; anti-glycan antibodies; biofilm; confocal microscopy; glycan microarray.

MeSH terms

  • Acetylation / drug effects
  • Animals
  • Anti-Bacterial Agents / chemistry
  • Anti-Bacterial Agents / pharmacology
  • Antibodies, Monoclonal / chemistry
  • Antibodies, Monoclonal / pharmacology
  • Biofilms* / drug effects
  • Female
  • Humans
  • Mice
  • Microbial Sensitivity Tests
  • Polysaccharides, Bacterial* / chemistry
  • Polysaccharides, Bacterial* / metabolism
  • Staphylococcal Infections / drug therapy
  • Staphylococcal Infections / pathology
  • Staphylococcus aureus* / drug effects
  • Staphylococcus aureus* / physiology

Substances

  • Polysaccharides, Bacterial
  • Antibodies, Monoclonal
  • Anti-Bacterial Agents
  • polysaccharide intercellular adhesin