Structure-function analyses of a pertussis-like toxin from pathogenic Escherichia coli reveal a distinct mechanism of inhibition of trimeric G-proteins

J Biol Chem. 2017 Sep 8;292(36):15143-15158. doi: 10.1074/jbc.M117.796094. Epub 2017 Jun 29.

Abstract

Pertussis-like toxins are secreted by several bacterial pathogens during infection. They belong to the AB5 virulence factors, which bind to glycans on host cell membranes for internalization. Host cell recognition and internalization are mediated by toxin B subunits sharing a unique pentameric ring-like assembly. Although the role of pertussis toxin in whooping cough is well-established, pertussis-like toxins produced by other bacteria are less studied, and their mechanisms of action are unclear. Here, we report that some extra-intestinal Escherichia coli pathogens (i.e. those that reside in the gut but can spread to other bodily locations) encode a pertussis-like toxin that inhibits mammalian cell growth in vitro We found that this protein, EcPlt, is related to toxins produced by both nontyphoidal and typhoidal Salmonella serovars. Pertussis-like toxins are secreted as disulfide-bonded heterohexamers in which the catalytic ADP-ribosyltransferase subunit is activated when exposed to the reducing environment in mammalian cells. We found here that the reduced EcPlt exhibits large structural rearrangements associated with its activation. We noted that inhibitory residues tethered within the NAD+-binding site by an intramolecular disulfide in the oxidized state dissociate upon the reduction and enable loop restructuring to form the nucleotide-binding site. Surprisingly, although pertussis toxin targets a cysteine residue within the α subunit of inhibitory trimeric G-proteins, we observed that activated EcPlt toxin modifies a proximal lysine/asparagine residue instead. In conclusion, our results reveal the molecular mechanism underpinning activation of pertussis-like toxins, and we also identified differences in host target specificity.

Keywords: ADP-ribosylation; Bordetella pertussis; Escherichia coli (E. coli); bacterial toxin; cholera toxin; host-pathogen interaction; toxin.

MeSH terms

  • Animals
  • Bacterial Toxins / chemistry*
  • Bacterial Toxins / pharmacology*
  • Cell Proliferation / drug effects
  • Chlorocebus aethiops
  • Dose-Response Relationship, Drug
  • Epithelial Cells / drug effects
  • Escherichia coli / chemistry*
  • HEK293 Cells
  • Heterotrimeric GTP-Binding Proteins / antagonists & inhibitors*
  • Heterotrimeric GTP-Binding Proteins / metabolism
  • Humans
  • Models, Molecular
  • Pertussis Toxin / chemistry*
  • Structure-Activity Relationship
  • Vero Cells

Substances

  • Bacterial Toxins
  • Pertussis Toxin
  • Heterotrimeric GTP-Binding Proteins

Associated data

  • PDB/3DQD