Botulinum neurotoxin serotype D attacks neurons via two carbohydrate-binding sites in a ganglioside-dependent manner

Biochem J. 2010 Oct 15;431(2):207-16. doi: 10.1042/BJ20101042.

Abstract

The extraordinarily high toxicity of botulinum neurotoxins primarily results from their specific binding and uptake into neurons. At motor neurons, the seven BoNT (botulinum neurotoxin) serotypes A-G inhibit acetylcholine release leading to flaccid paralysis. Uptake of BoNT/A, B, E, F and G requires a dual interaction with gangliosides and the synaptic vesicle proteins synaptotagmin or SV2 (synaptic vesicle glycoprotein 2), whereas little is known about the cell entry mechanisms of the serotypes C and D, which display the lowest amino acid sequence identity compared with the other five serotypes. In the present study we demonstrate that the neurotoxicity of BoNT/D depends on the presence of gangliosides by employing phrenic nerve hemidiaphragm preparations derived from mice expressing the gangliosides GM3, GM2, GM1 and GD1a, or only GM3 [a description of our use of ganglioside nomenclature is given in Svennerholm (1994) Prog. Brain Res. 101, XI-XIV]. High-resolution crystal structures of the 50 kDa cell-binding domain of BoNT/D alone and in complex with sialic acid, as well as biological analyses of single-site BoNT/D mutants identified two carbohydrate-binding sites. One site is located at a position previously identified in BoNT/A, B, E, F and G, but is lacking the conserved SXWY motif. The other site, co-ordinating one molecule of sialic acid, resembles the second ganglioside-binding pocket (the sialic-acid-binding site) of TeNT (tetanus neurotoxin).

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
  • Binding Sites
  • Biological Assay
  • Botulinum Toxins / chemistry*
  • Botulinum Toxins / metabolism
  • Botulinum Toxins / toxicity*
  • Carbohydrate Sequence
  • Carbohydrates / chemistry*
  • Cell Membrane / drug effects
  • Cell Membrane / metabolism
  • Crystallography, X-Ray
  • Gangliosides / chemistry
  • Gangliosides / metabolism*
  • Mice
  • Models, Molecular
  • Mutagenesis, Site-Directed
  • Mutant Proteins / chemistry
  • Mutant Proteins / metabolism
  • N-Acetylneuraminic Acid / chemistry
  • Neurons / drug effects*
  • Neurons / pathology
  • Peptide Fragments / chemistry
  • Phrenic Nerve / drug effects
  • Phrenic Nerve / metabolism
  • Phrenic Nerve / pathology
  • Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization
  • Synaptosomes / drug effects
  • Synaptosomes / metabolism

Substances

  • Carbohydrates
  • Gangliosides
  • Mutant Proteins
  • Peptide Fragments
  • botulinum toxin type D
  • Botulinum Toxins
  • N-Acetylneuraminic Acid