A natural product inhibits the initiation of α-synuclein aggregation and suppresses its toxicity

Proc Natl Acad Sci U S A. 2017 Feb 7;114(6):E1009-E1017. doi: 10.1073/pnas.1610586114. Epub 2017 Jan 17.

Abstract

The self-assembly of α-synuclein is closely associated with Parkinson's disease and related syndromes. We show that squalamine, a natural product with known anticancer and antiviral activity, dramatically affects α-synuclein aggregation in vitro and in vivo. We elucidate the mechanism of action of squalamine by investigating its interaction with lipid vesicles, which are known to stimulate nucleation, and find that this compound displaces α-synuclein from the surfaces of such vesicles, thereby blocking the first steps in its aggregation process. We also show that squalamine almost completely suppresses the toxicity of α-synuclein oligomers in human neuroblastoma cells by inhibiting their interactions with lipid membranes. We further examine the effects of squalamine in a Caenorhabditis elegans strain overexpressing α-synuclein, observing a dramatic reduction of α-synuclein aggregation and an almost complete elimination of muscle paralysis. These findings suggest that squalamine could be a means of therapeutic intervention in Parkinson's disease and related conditions.

Keywords: Parkinson’s disease; amyloid formation; drug development; protein aggregation; toxic oligomers.

Publication types

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

MeSH terms

  • Algorithms
  • Amino Acid Sequence
  • Animals
  • Animals, Genetically Modified
  • Biological Products / chemistry
  • Biological Products / pharmacology
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / metabolism
  • Cell Line, Tumor
  • Cholestanols / chemistry
  • Cholestanols / pharmacology
  • Humans
  • Membrane Lipids / chemistry
  • Membrane Lipids / metabolism
  • Molecular Structure
  • Neuroblastoma / metabolism
  • Neuroblastoma / pathology
  • Paresis / genetics
  • Paresis / metabolism
  • Paresis / prevention & control
  • Parkinson Disease / metabolism
  • Protein Aggregates / drug effects*
  • Protein Aggregation, Pathological / prevention & control*
  • Protein Binding / drug effects
  • Protein Multimerization / drug effects
  • alpha-Synuclein / chemistry*
  • alpha-Synuclein / genetics
  • alpha-Synuclein / metabolism

Substances

  • Biological Products
  • Cholestanols
  • Membrane Lipids
  • Protein Aggregates
  • alpha-Synuclein
  • squalamine