Galectin-3 Is a Target for Proteases Involved in the Virulence of Staphylococcus aureus

Infect Immun. 2017 Jun 20;85(7):e00177-17. doi: 10.1128/IAI.00177-17. Print 2017 Jul.

Abstract

Staphylococcus aureus is a major cause of skin and soft tissue infection. The bacterium expresses four major proteases that are emerging as virulence factors: aureolysin (Aur), V8 protease (SspA), staphopain A (ScpA), and staphopain B (SspB). We hypothesized that human galectin-3, a β-galactoside-binding lectin involved in immune regulation and antimicrobial defense, is a target for these proteases and that proteolysis of galectin-3 is a novel immune evasion mechanism. Indeed, supernatants from laboratory strains and clinical isolates of S. aureus caused galectin-3 degradation. Similar proteolytic capacities were found in Staphylococcus epidermidis isolates but not in Staphylococcus saprophyticus Galectin-3-induced activation of the neutrophil NADPH oxidase was abrogated by bacterium-derived proteolysis of galectin-3, and SspB was identified as the major protease responsible. The impact of galectin-3 and protease expression on S. aureus virulence was studied in a murine skin infection model. In galectin-3+/+ mice, SspB-expressing S. aureus caused larger lesions and resulted in higher bacterial loads than protease-lacking bacteria. No such difference in bacterial load or lesion size was detected in galectin-3-/- mice, which overall showed smaller lesion sizes than the galectin-3+/+ animals. In conclusion, the staphylococcal protease SspB inactivates galectin-3, abrogating its stimulation of oxygen radical production in human neutrophils and increasing tissue damage during skin infection.

Keywords: Staphylococcus aureus; galectin-3; neutrophils; protease; skin infection; staphopain; virulence; virulence factors; virulence regulation.

MeSH terms

  • Animals
  • Bacterial Load
  • Bacterial Proteins / metabolism*
  • Blood Proteins
  • Disease Models, Animal
  • Galectin 3 / metabolism*
  • Galectins
  • Host-Pathogen Interactions*
  • Humans
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Proteolysis
  • Serine Endopeptidases / metabolism*
  • Staphylococcal Skin Infections / microbiology
  • Staphylococcal Skin Infections / pathology
  • Staphylococcus aureus / enzymology*
  • Staphylococcus aureus / pathogenicity*
  • Virulence

Substances

  • Bacterial Proteins
  • Blood Proteins
  • Galectin 3
  • Galectins
  • LGALS3 protein, human
  • Serine Endopeptidases
  • sspB protein, Staphylococcus aureus