A small-molecule Nrf1 and Nrf2 activator mitigates polyglutamine toxicity in spinal and bulbar muscular atrophy

Hum Mol Genet. 2016 May 15;25(10):1979-1989. doi: 10.1093/hmg/ddw073. Epub 2016 Mar 8.

Abstract

Spinal and bulbar muscular atrophy (SBMA, also known as Kennedy's disease) is one of nine neurodegenerative disorders that are caused by expansion of polyglutamine-encoding CAG repeats. Intracellular accumulation of abnormal proteins in these diseases, a pathological hallmark, is associated with defects in protein homeostasis. Enhancement of the cellular proteostasis capacity with small molecules has therefore emerged as a promising approach to treatment. Here, we characterize a novel curcumin analog, ASC-JM17, as an activator of central pathways controlling protein folding, degradation and oxidative stress resistance. ASC-JM17 acts on Nrf1, Nrf2 and Hsf1 to increase the expression of proteasome subunits, antioxidant enzymes and molecular chaperones. We show that ASC-JM17 ameliorates toxicity of the mutant androgen receptor (AR) responsible for SBMA in cell, fly and mouse models. Knockdown of the Drosophila Nrf1 and Nrf2 ortholog cap 'n' collar isoform-C, but not Hsf1, blocks the protective effect of ASC-JM17 on mutant AR-induced eye degeneration in flies. Our observations indicate that activation of the Nrf1/Nrf2 pathway is a viable option for pharmacological intervention in SBMA and potentially other polyglutamine diseases.

Publication types

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

MeSH terms

  • Animals
  • Bulbo-Spinal Atrophy, X-Linked / drug therapy
  • Bulbo-Spinal Atrophy, X-Linked / genetics*
  • Bulbo-Spinal Atrophy, X-Linked / pathology
  • Curcumin / administration & dosage
  • Curcumin / analogs & derivatives*
  • Curcumin / chemistry
  • DNA-Binding Proteins / genetics*
  • Disease Models, Animal
  • Drosophila Proteins / genetics*
  • Drosophila melanogaster / genetics
  • Gene Knockdown Techniques
  • Heat Shock Transcription Factors
  • Humans
  • Mice
  • Muscular Disorders, Atrophic / drug therapy
  • Muscular Disorders, Atrophic / genetics*
  • Muscular Disorders, Atrophic / pathology
  • NF-E2-Related Factor 1 / genetics*
  • NF-E2-Related Factor 2 / genetics*
  • Oxidative Stress / drug effects
  • Peptides / genetics
  • Proteasome Endopeptidase Complex / drug effects
  • Protein Aggregation, Pathological / genetics
  • Protein Folding / drug effects
  • Receptors, Androgen / genetics*
  • Signal Transduction / drug effects
  • Small Molecule Libraries / administration & dosage
  • Transcription Factors / genetics*
  • Trinucleotide Repeat Expansion / genetics*

Substances

  • AR protein, human
  • ASC-JM17
  • DNA-Binding Proteins
  • Drosophila Proteins
  • Heat Shock Transcription Factors
  • Hsf protein, Drosophila
  • NF-E2-Related Factor 1
  • NF-E2-Related Factor 2
  • Peptides
  • Receptors, Androgen
  • Small Molecule Libraries
  • Transcription Factors
  • polyglutamine
  • Proteasome Endopeptidase Complex
  • Curcumin