A Dual Microscopy-Based Assay To Assess Listeria monocytogenes Cellular Entry and Vacuolar Escape

Appl Environ Microbiol. 2015 Oct 23;82(1):211-7. doi: 10.1128/AEM.02302-15. Print 2016 Jan 1.

Abstract

Listeria monocytogenes is a Gram-positive bacterium and a facultative intracellular pathogen that invades mammalian cells, disrupts its internalization vacuole, and proliferates in the host cell cytoplasm. Here, we describe a novel image-based microscopy assay that allows discrimination between cellular entry and vacuolar escape, enabling high-content screening to identify factors specifically involved in these two steps. We first generated L. monocytogenes and Listeria innocua strains expressing a β-lactamase covalently attached to the bacterial cell wall. These strains were then incubated with HeLa cells containing the Förster resonance energy transfer (FRET) probe CCF4 in their cytoplasm. The CCF4 probe was cleaved by the bacterial surface β-lactamase only in cells inoculated with L. monocytogenes but not those inoculated with L. innocua, thereby demonstrating bacterial access to the host cytoplasm. Subsequently, we performed differential immunofluorescence staining to distinguish extracellular versus total bacterial populations in samples that were also analyzed by the FRET-based assay. With this two-step analysis, bacterial entry can be distinguished from vacuolar rupture in a single experiment. Our novel approach represents a powerful tool for identifying factors that determine the intracellular niche of L. monocytogenes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacterial Proteins / metabolism
  • Cytoplasm / microbiology*
  • Fluorescence Resonance Energy Transfer
  • HeLa Cells
  • Heterocyclic Compounds, 4 or More Rings / metabolism
  • Host-Pathogen Interactions*
  • Humans
  • Listeria / enzymology
  • Listeria / metabolism
  • Listeria monocytogenes / enzymology
  • Listeria monocytogenes / physiology*
  • Microscopy, Fluorescence
  • Vacuoles / microbiology*
  • beta-Lactamases / metabolism

Substances

  • Bacterial Proteins
  • CCF4-AM
  • Heterocyclic Compounds, 4 or More Rings
  • beta-Lactamases