Induction of α-synuclein aggregate formation by CSF exosomes from patients with Parkinson's disease and dementia with Lewy bodies

Brain. 2016 Feb;139(Pt 2):481-94. doi: 10.1093/brain/awv346. Epub 2015 Dec 8.

Abstract

Extracellular α-synuclein has been proposed as a crucial mechanism for induction of pathological aggregate formation in previously healthy cells. In vitro, extracellular α-synuclein is partially associated with exosomal vesicles. Recently, we have provided evidence that exosomal α-synuclein is present in the central nervous system in vivo. We hypothesized that exosomal α-synuclein species from patients with α-synuclein related neurodegeneration serve as carriers for interneuronal disease transmission. We isolated exosomes from cerebrospinal fluid from patients with Parkinson's disease, dementia with Lewy bodies, progressive supranuclear palsy as a non-α-synuclein related disorder that clinically overlaps with Parkinson's disease, and neurological controls. Cerebrospinal fluid exosome numbers, α-synuclein protein content of cerebrospinal fluid exosomes and their potential to induce oligomerization of α-synuclein were analysed. The quantification of cerebrospinal fluid exosomal α-synuclein showed distinct differences between patients with Parkinson's disease and dementia with Lewy bodies. In addition, exosomal α-synuclein levels correlated with the severity of cognitive impairment in cross-sectional samples from patients with dementia with Lewy bodies. Importantly, cerebrospinal fluid exosomes derived from Parkinson's disease and dementia with Lewy bodies induce oligomerization of α-synuclein in a reporter cell line in a dose-dependent manner. Our data suggest that cerebrospinal fluid exosomes from patients with Parkinson's disease and dementia with Lewy bodies contain a pathogenic species of α-synuclein, which could initiate oligomerization of soluble α-synuclein in target cells and confer disease pathology.

Keywords: Parkinson’s disease; cerebrospinal fluid; exosomes; extracellular vesicles; α-synuclein.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cerebrospinal Fluid* / metabolism
  • Cohort Studies
  • Cross-Sectional Studies
  • Exosomes* / metabolism
  • Female
  • Follow-Up Studies
  • Humans
  • Lewy Body Disease / cerebrospinal fluid*
  • Lewy Body Disease / metabolism
  • Longitudinal Studies
  • Male
  • Parkinson Disease / cerebrospinal fluid*
  • Parkinson Disease / metabolism
  • Protein Aggregates / physiology*
  • alpha-Synuclein / biosynthesis
  • alpha-Synuclein / cerebrospinal fluid*

Substances

  • Protein Aggregates
  • alpha-Synuclein