In vitro evolution driven by epistasis reveals alternative cholesterol-specific binding motifs of perfringolysin O

J Biol Chem. 2024 Sep;300(9):107664. doi: 10.1016/j.jbc.2024.107664. Epub 2024 Aug 14.

Abstract

The crucial molecular factors that shape the interfaces of lipid-binding proteins with their target ligands and surfaces remain unknown due to the complex makeup of biological membranes. Cholesterol, the major modulator of bilayer structure in mammalian cell membranes, is recognized by various proteins, including the well-studied cholesterol-dependent cytolysins. Here, we use in vitro evolution to investigate the molecular adaptations that preserve the cholesterol specificity of perfringolysin O, the prototypical cholesterol-dependent cytolysin from Clostridium perfringens. We identify variants with altered membrane-binding interfaces whose cholesterol-specific activity exceeds that of the wild-type perfringolysin O. These novel variants represent alternative evolutionary outcomes and have mutations at conserved positions that can only accumulate when epistatic constraints are alleviated. Our results improve the current understanding of the biochemical malleability of the surface of a lipid-binding protein.

Keywords: cholesterol specificity; directed evolution; lipid specificity; pore forming toxins; ribosome display.

MeSH terms

  • Amino Acid Motifs
  • Bacterial Toxins* / chemistry
  • Bacterial Toxins* / genetics
  • Bacterial Toxins* / metabolism
  • Cholesterol* / genetics
  • Cholesterol* / metabolism
  • Clostridium perfringens* / genetics
  • Clostridium perfringens* / metabolism
  • Epistasis, Genetic
  • Hemolysin Proteins* / chemistry
  • Hemolysin Proteins* / genetics
  • Hemolysin Proteins* / metabolism
  • Mutation
  • Protein Binding

Substances

  • Hemolysin Proteins
  • Cholesterol
  • Clostridium perfringens theta-toxin
  • Bacterial Toxins