Interaction between Staphylococcus Agr virulence and neutrophils regulates pathogen expansion in the skin

Cell Host Microbe. 2021 Jun 9;29(6):930-940.e4. doi: 10.1016/j.chom.2021.03.007. Epub 2021 Apr 13.

Abstract

Staphylococcus aureus commonly infects the skin, but the host-pathogen interactions controlling bacterial growth remain unclear. S. aureus virulence is regulated by the Agr quorum-sensing system that controls factors including phenol-soluble modulins (PSMs), a group of cytotoxic peptides. We found a differential requirement for Agr and PSMα for pathogen growth in the skin. In neutrophil-deficient mice, S. aureus growth on the epidermis was unaffected, but the pathogen penetrated the dermis through mechanisms that require PSMα. In the dermis, pathogen expansion required Agr in wild-type mice, but not in neutrophil-deficient mice. Agr limited oxidative and non-oxidative killing in neutrophils by inhibiting pathogen late endosome localization and promoting phagosome escape. Unlike Agr, the SaeR/S virulence program was dispensable for growth in the epidermis and promoted dermal pathogen expansion independently of neutrophils. Thus, S. aureus growth and invasion are differentially regulated with Agr limiting intracellular killing within neutrophils to promote pathogen expansion in the dermis and subcutaneous tissue.

Keywords: Agr virulence; SaeR/S virulence; Staphylococcus aureus; neutrophils; phenol-soluble modulins; skin infection; skin inflammation.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bacterial Proteins / metabolism*
  • Bacterial Toxins / metabolism
  • Host-Pathogen Interactions
  • Humans
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mutation
  • Neutrophils / physiology*
  • Protein Kinases / metabolism
  • Quorum Sensing
  • Skin / microbiology*
  • Staphylococcal Infections / microbiology*
  • Staphylococcus aureus / pathogenicity*
  • Staphylococcus aureus / physiology*
  • Trans-Activators / metabolism*
  • Transcription Factors / metabolism
  • Virulence*

Substances

  • Agr protein, Staphylococcus aureus
  • Bacterial Proteins
  • Bacterial Toxins
  • SaeR protein, Staphylococcus aureus
  • Trans-Activators
  • Transcription Factors
  • staphylococcal delta toxin
  • Protein Kinases
  • SaeS protein, Staphylococcus aureus