Mutual exacerbation of peroxisome proliferator-activated receptor γ coactivator 1α deregulation and α-synuclein oligomerization

Ann Neurol. 2015 Jan;77(1):15-32. doi: 10.1002/ana.24294. Epub 2014 Dec 19.

Abstract

Objective: Aggregation of α-synuclein (α-syn) and α-syn cytotoxicity are hallmarks of sporadic and familial Parkinson disease (PD), with accumulating evidence that prefibrillar oligomers and protofibrils are the pathogenic species in PD and related synucleinopathies. Peroxisome proliferator-activated receptor γ coactivator 1α (PGC-1α), a key regulator of mitochondrial biogenesis and cellular energy metabolism, has recently been associated with the pathophysiology of PD. Despite extensive effort on studying the function of PGC-1α in mitochondria, no studies have addressed whether PGC-1α directly influences oligomerization of α-syn or whether α-syn oligomers impact PGC-1α expression.

Materials and methods: We tested whether pharmacological or genetic activation of PGC-1α or PGC-11α knockdown could modulate the oligomerization of α-syn in vitro by using an α-syn -fragment complementation assay.

Results: In this study, we found that both PGC-1α reference gene (RG-PGC-1α) and the central nervous system (CNS)-specific PGC-1α (CNS-PGC-1α) are downregulated in human PD brain, in A30P α-syn transgenic animals, and in a cell culture model for α-syn oligomerization. Importantly, downregulation of both RG-PGC-1α and CNS-PGC-1α in cell culture or neurons from RG-PGC-1α-deficient mice leads to a strong induction of α-syn oligomerization and toxicity. In contrast, pharmacological activation or genetic overexpression of RG-PGC-1α reduced α-syn oligomerization and rescued α-syn-mediated toxicity.

Interpretation: Based on our results, we propose that PGC-1α downregulation and α-syn oligomerization form a vicious circle, thereby influencing and/or potentiating each other. Our data indicate that restoration of PGC-1α is a promising approach for development of effective drugs for the treatment of PD and related synucleinopathies.

Publication types

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

MeSH terms

  • Aged
  • Aged, 80 and over
  • Animals
  • Cells, Cultured
  • Cerebral Cortex / cytology
  • Disease Models, Animal
  • Embryo, Mammalian
  • Enzyme Inhibitors / pharmacology
  • Female
  • Gene Expression Regulation / drug effects
  • Gene Expression Regulation / genetics*
  • Glioma / pathology
  • Humans
  • Macrolides / pharmacology
  • Male
  • Mice
  • Mice, Transgenic
  • Middle Aged
  • Neurons / metabolism
  • PPAR gamma / genetics*
  • PPAR gamma / metabolism*
  • Parkinson Disease / pathology
  • Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha
  • RNA Polymerase II / genetics
  • RNA Polymerase II / metabolism
  • Resveratrol
  • Stilbenes / pharmacology
  • Substantia Nigra / metabolism*
  • TATA-Box Binding Protein / genetics
  • TATA-Box Binding Protein / metabolism
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*
  • alpha-Synuclein / genetics
  • alpha-Synuclein / metabolism*

Substances

  • Enzyme Inhibitors
  • Macrolides
  • PPAR gamma
  • Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha
  • Ppargc1a protein, mouse
  • Stilbenes
  • TATA-Box Binding Protein
  • Transcription Factors
  • alpha-Synuclein
  • bafilomycin A1
  • RNA Polymerase II
  • Resveratrol