α-synuclein-lipoprotein interactions and elevated ApoE level in cerebrospinal fluid from Parkinson's disease patients

Proc Natl Acad Sci U S A. 2019 Jul 23;116(30):15226-15235. doi: 10.1073/pnas.1821409116. Epub 2019 Jul 3.

Abstract

The progressive accumulation, aggregation, and spread of α-synuclein (αSN) are common hallmarks of Parkinson's disease (PD) pathology. Moreover, numerous proteins interact with αSN species, influencing its toxicity in the brain. In the present study, we extended analyses of αSN-interacting proteins to cerebrospinal fluid (CSF). Using coimmunoprecipitation, followed by mass spectrometry, we found that αSN colocalize with apolipoproteins on lipoprotein vesicles. We confirmed these interactions using several methods, including the enrichment of lipoproteins with a recombinant αSN, and the subsequent uptake of prepared vesicles by human dopaminergic neuronal-like cells. Further, we report an increased level of ApoE in CSF from early PD patients compared with matched controls in 3 independent cohorts. Moreover, in contrast to controls, we observed the presence of ApoE-positive neuromelanin-containing dopaminergic neurons in substantia nigra of PD patients. In conclusion, the cooccurrence of αSN on lipoprotein vesicles, and their uptake by dopaminergic neurons along with an increase of ApoE in early PD, proposes a mechanism(s) for αSN spreading in the extracellular milieu of PD.

Keywords: Parkinson's disease; apolipoproteins; cerebrospinal fluid; α-synuclein.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aged
  • Amino Acid Sequence
  • Apolipoproteins / cerebrospinal fluid*
  • Apolipoproteins / genetics
  • Apolipoproteins E / cerebrospinal fluid*
  • Apolipoproteins E / genetics
  • Case-Control Studies
  • Cohort Studies
  • Dopaminergic Neurons / metabolism*
  • Dopaminergic Neurons / pathology
  • Female
  • Gene Expression
  • Humans
  • Male
  • Melanins / cerebrospinal fluid
  • Melanins / genetics
  • Middle Aged
  • Parkinson Disease / cerebrospinal fluid*
  • Parkinson Disease / genetics
  • Parkinson Disease / pathology
  • Protein Binding
  • Protein Transport
  • Sequence Alignment
  • Sequence Homology, Amino Acid
  • Substantia Nigra / metabolism*
  • Substantia Nigra / pathology
  • Transport Vesicles / metabolism
  • alpha-Synuclein / cerebrospinal fluid*
  • alpha-Synuclein / genetics

Substances

  • Apolipoproteins
  • Apolipoproteins E
  • Melanins
  • SNCA protein, human
  • alpha-Synuclein
  • neuromelanin