Dual modes of membrane binding direct pore formation by Streptolysin O

Mol Microbiol. 2015 Sep;97(6):1036-50. doi: 10.1111/mmi.13085. Epub 2015 Jul 4.

Abstract

Effector translocation is central to the virulence of many bacterial pathogens, including Streptococcus pyogenes, which utilizes the cholesterol-dependent cytolysin Streptolysin O (SLO) to translocate the NAD(+) glycohydrolase SPN into host cells during infection. SLO's translocation activity does not require host cell membrane cholesterol or pore formation by SLO, yet SLO does form pores during infection via a cholesterol-dependent mechanism. Although cholesterol was considered the primary receptor for SLO, SLO's membrane-binding domain also encodes a putative carbohydrate-binding site, implicating a potential glycan receptor in binding and pore formation. Analysis of carbohydrate-binding site SLO mutants and carbohydrate-defective cell lines revealed that glycan recognition is involved in SLO's pore formation pathway and is an essential step when SLO is secreted by non-adherent bacteria, as occurs during lysis of erythrocytes. However, SLO also recognizes host cell membranes via a second mechanism when secreted from adherent bacteria, which requires co-secretion of SPN but not glycan binding by SLO. This SPN-mediated membrane binding of SLO correlates with SPN translocation, and requires SPN's non-enzymatic domain, which is predicted to adopt the structure of a carbohydrate-binding module. SPN-dependent membrane binding also promotes pore formation by SLO, demonstrating that pore formation can occur by distinct pathways during infection.

Publication types

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

MeSH terms

  • Animals
  • Bacterial Infections / metabolism
  • Bacterial Proteins / chemistry
  • Bacterial Proteins / metabolism
  • CHO Cells
  • Carbohydrate Metabolism
  • Cell Membrane / metabolism*
  • Cholesterol / metabolism
  • Cricetulus
  • Escherichia coli / cytology
  • Escherichia coli / metabolism
  • Hemolysis
  • Mutation
  • NAD+ Nucleosidase / genetics
  • NAD+ Nucleosidase / metabolism
  • Protein Binding
  • Protein Transport
  • Streptococcus pyogenes / cytology*
  • Streptococcus pyogenes / metabolism
  • Streptolysins / chemistry
  • Streptolysins / metabolism*

Substances

  • Bacterial Proteins
  • Streptolysins
  • streptolysin O
  • Cholesterol
  • NAD+ Nucleosidase