Synaptotagmins I and II mediate entry of botulinum neurotoxin B into cells

J Cell Biol. 2003 Sep 29;162(7):1293-303. doi: 10.1083/jcb.200305098. Epub 2003 Sep 22.

Abstract

Botulinum neurotoxins (BoNTs) cause botulism by entering neurons and cleaving proteins that mediate neurotransmitter release; disruption of exocytosis results in paralysis and death. The receptors for BoNTs are thought to be composed of both proteins and gangliosides; however, protein components that mediate toxin entry have not been identified. Using gain-of-function and loss-of-function approaches, we report here that the secretory vesicle proteins, synaptotagmins (syts) I and II, mediate the entry of BoNT/B (but not BoNT/A or E) into PC12 cells. Further, we demonstrate that BoNT/B entry into PC12 cells and rat diaphragm motor nerve terminals was activity dependent and can be blocked using fragments of syt II that contain the BoNT/B-binding domain. Finally, we show that syt II fragments, in conjunction with gangliosides, neutralized BoNT/B in intact mice. These findings establish that syts I and II can function as protein receptors for BoNT/B.

Publication types

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

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Botulinum Toxins / pharmacokinetics*
  • Botulinum Toxins, Type A
  • Botulism / metabolism*
  • Calcium-Binding Proteins*
  • Cytoplasmic Vesicles / metabolism
  • Female
  • Gangliosides / metabolism
  • Membrane Glycoproteins / chemistry
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / metabolism*
  • Mice
  • Molecular Sequence Data
  • Motor Neurons / metabolism
  • Nerve Tissue Proteins / chemistry
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism*
  • PC12 Cells
  • Protein Structure, Tertiary
  • Rats
  • Synaptotagmin II
  • Synaptotagmins

Substances

  • Calcium-Binding Proteins
  • Gangliosides
  • Membrane Glycoproteins
  • Nerve Tissue Proteins
  • Synaptotagmin II
  • Syt2 protein, mouse
  • Syt2 protein, rat
  • rimabotulinumtoxinB
  • Synaptotagmins
  • Botulinum Toxins
  • Botulinum Toxins, Type A