Aberrant regulation of the GSK-3β/NRF2 axis unveils a novel therapy for adrenoleukodystrophy

EMBO Mol Med. 2018 Aug;10(8):e8604. doi: 10.15252/emmm.201708604.

Abstract

The nuclear factor erythroid 2-like 2 (NRF2) is the master regulator of endogenous antioxidant responses. Oxidative damage is a shared and early-appearing feature in X-linked adrenoleukodystrophy (X-ALD) patients and the mouse model (Abcd1 null mouse). This rare neurometabolic disease is caused by the loss of function of the peroxisomal transporter ABCD1, leading to an accumulation of very long-chain fatty acids and the induction of reactive oxygen species of mitochondrial origin. Here, we identify an impaired NRF2 response caused by aberrant activity of GSK-3β. We find that GSK-3β inhibitors can significantly reactivate the blunted NRF2 response in patients' fibroblasts. In the mouse models (Abcd1- and Abcd1-/Abcd2-/- mice), oral administration of dimethyl fumarate (DMF/BG12/Tecfidera), an NRF2 activator in use for multiple sclerosis, normalized (i) mitochondrial depletion, (ii) bioenergetic failure, (iii) oxidative damage, and (iv) inflammation, highlighting an intricate cross-talk governing energetic and redox homeostasis in X-ALD Importantly, DMF halted axonal degeneration and locomotor disability suggesting that therapies activating NRF2 hold therapeutic potential for X-ALD and other axonopathies with impaired GSK-3β/NRF2 axis.

Keywords: GSK‐3; NRF2; adrenoleukodystrophy; dimethyl fumarate; oxidative stress.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • ATP Binding Cassette Transporter, Subfamily D, Member 1 / genetics
  • Adrenoleukodystrophy / drug therapy*
  • Adrenoleukodystrophy / metabolism
  • Animals
  • Anti-Inflammatory Agents / therapeutic use
  • Antioxidants / therapeutic use*
  • Dimethyl Fumarate / administration & dosage
  • Dimethyl Fumarate / therapeutic use*
  • Disease Models, Animal
  • Gliosis / drug therapy
  • Glycogen Synthase Kinase 3 beta / metabolism*
  • Humans
  • Male
  • Mice
  • Mice, Knockout
  • NF-E2-Related Factor 2 / metabolism*
  • Organelle Biogenesis
  • Oxidative Stress / physiology
  • Proto-Oncogene Proteins c-akt / metabolism
  • Reactive Oxygen Species / metabolism

Substances

  • ATP Binding Cassette Transporter, Subfamily D, Member 1
  • Abcd1 protein, mouse
  • Anti-Inflammatory Agents
  • Antioxidants
  • NF-E2-Related Factor 2
  • NFE2L2 protein, human
  • Nfe2l2 protein, mouse
  • Reactive Oxygen Species
  • Glycogen Synthase Kinase 3 beta
  • Proto-Oncogene Proteins c-akt
  • Dimethyl Fumarate