α-Synuclein stimulation of monoamine oxidase-B and legumain protease mediates the pathology of Parkinson's disease

EMBO J. 2018 Jun 15;37(12):e98878. doi: 10.15252/embj.201798878. Epub 2018 May 16.

Abstract

Dopaminergic neurodegeneration in Parkinson's disease (PD) is associated with abnormal dopamine metabolism by MAO-B (monoamine oxidase-B) and intracellular α-Synuclein (α-Syn) aggregates, called the Lewy body. However, the molecular relationship between α-Syn and MAO-B remains unclear. Here, we show that α-Syn directly binds to MAO-B and stimulates its enzymatic activity, which triggers AEP (asparagine endopeptidase; legumain) activation and subsequent α-Syn cleavage at N103, leading to dopaminergic neurodegeneration. Interestingly, the dopamine metabolite, DOPAL, strongly activates AEP, and the N103 fragment of α-Syn binds and activates MAO-B. Accordingly, overexpression of AEP in SNCA transgenic mice elicits α-Syn N103 cleavage and accelerates PD pathogenesis, and inhibition of MAO-B by Rasagiline diminishes α-Syn-mediated PD pathology and motor dysfunction. Moreover, virally mediated expression of α-Syn N103 induces PD pathogenesis in wild-type, but not MAO-B-null mice. Our findings thus support that AEP-mediated cleavage of α-Syn at N103 is required for the association and activation of MAO-B, mediating PD pathogenesis.

Keywords: DOPAL; MPTP; delta‐secretase (AEP); neurodegenerative diseases.

Publication types

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

MeSH terms

  • Animals
  • Cysteine Endopeptidases / genetics
  • Cysteine Endopeptidases / metabolism*
  • Disease Models, Animal
  • Dopamine / genetics
  • Dopamine / metabolism
  • Indans / pharmacology
  • Mice
  • Mice, Transgenic
  • Monoamine Oxidase / genetics
  • Monoamine Oxidase / metabolism*
  • Monoamine Oxidase Inhibitors / pharmacology
  • Parkinson Disease / genetics
  • Parkinson Disease / metabolism*
  • Parkinson Disease / pathology
  • alpha-Synuclein / genetics
  • alpha-Synuclein / metabolism*

Substances

  • Indans
  • Monoamine Oxidase Inhibitors
  • Snca protein, mouse
  • alpha-Synuclein
  • rasagiline
  • Monoamine Oxidase
  • Cysteine Endopeptidases
  • asparaginylendopeptidase
  • Dopamine