Structure of a bimodular botulinum neurotoxin complex provides insights into its oral toxicity

PLoS Pathog. 2013;9(10):e1003690. doi: 10.1371/journal.ppat.1003690. Epub 2013 Oct 10.

Abstract

Botulinum neurotoxins (BoNTs) are produced by Clostridium botulinum and cause the fatal disease botulism, a flaccid paralysis of the muscle. BoNTs are released together with several auxiliary proteins as progenitor toxin complexes (PTCs) to become highly potent oral poisons. Here, we report the structure of a ∼760 kDa 14-subunit large PTC of serotype A (L-PTC/A) and reveal insight into its absorption mechanism. Using a combination of X-ray crystallography, electron microscopy, and functional studies, we found that L-PTC/A consists of two structurally and functionally independent sub-complexes. A hetero-dimeric 290 kDa complex protects BoNT, while a hetero-dodecameric 470 kDa complex facilitates its absorption in the harsh environment of the gastrointestinal tract. BoNT absorption is mediated by nine glycan-binding sites on the dodecameric sub-complex that forms multivalent interactions with carbohydrate receptors on intestinal epithelial cells. We identified monosaccharides that blocked oral BoNT intoxication in mice, which suggests a new strategy for the development of preventive countermeasures for BoNTs based on carbohydrate receptor mimicry.

Publication types

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

MeSH terms

  • Animals
  • Botulinum Toxins* / chemistry
  • Botulinum Toxins* / genetics
  • Botulinum Toxins* / toxicity
  • Botulism*
  • Clostridium botulinum / genetics
  • Clostridium botulinum / metabolism
  • Female
  • Mice
  • Multiprotein Complexes* / chemistry
  • Multiprotein Complexes* / genetics
  • Multiprotein Complexes* / toxicity
  • Protein Structure, Quaternary
  • Structure-Activity Relationship

Substances

  • Multiprotein Complexes
  • Botulinum Toxins