Glutathione S-Transferase Regulates Mitochondrial Populations in Axons through Increased Glutathione Oxidation

Neuron. 2019 Jul 3;103(1):52-65.e6. doi: 10.1016/j.neuron.2019.04.017. Epub 2019 May 14.

Abstract

Mitochondria are essential in long axons to provide metabolic support and sustain neuron integrity. A healthy mitochondrial pool is maintained by biogenesis, transport, mitophagy, fission, and fusion, but how these events are regulated in axons is not well defined. Here, we show that the Drosophila glutathione S-transferase (GST) Gfzf prevents mitochondrial hyperfusion in axons. Gfzf loss altered redox balance between glutathione (GSH) and oxidized glutathione (GSSG) and initiated mitochondrial fusion through the coordinated action of Mfn and Opa1. Gfzf functioned epistatically with the thioredoxin peroxidase Jafrac1 and the thioredoxin reductase 1 TrxR-1 to regulate mitochondrial dynamics. Altering GSH:GSSG ratios in mouse primary neurons in vitro also induced hyperfusion. Mitochondrial changes caused deficits in trafficking, the metabolome, and neuronal physiology. Changes in GSH and oxidative state are associated with neurodegenerative diseases like Alzheimer's. Our demonstration that GSTs are key in vivo regulators of axonal mitochondrial length and number provides a potential mechanistic link.

Keywords: Drosophila; Gfzf; axons; glutathione; glutathione S-transferases; marf; mitochondria; mitofusin; neurons; redox.

Publication types

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

MeSH terms

  • Animals
  • Axons / physiology*
  • Axons / ultrastructure
  • Carrier Proteins / physiology*
  • Drosophila
  • Drosophila Proteins / genetics
  • Drosophila Proteins / physiology
  • Female
  • Glutathione / metabolism*
  • Membrane Proteins / genetics
  • Membrane Proteins / physiology
  • Mice
  • Mice, Inbred C57BL
  • Mitochondria / physiology*
  • Neurons / metabolism
  • Oxidation-Reduction
  • Peroxidases / genetics
  • Peroxidases / physiology
  • Pregnancy
  • Primary Cell Culture
  • Thioredoxin Reductase 1 / genetics
  • Thioredoxin Reductase 1 / physiology

Substances

  • Carrier Proteins
  • Drosophila Proteins
  • GFZF protein, Drosophila
  • Marf protein, Drosophila
  • Membrane Proteins
  • OPA1 protein, Drosophila
  • Jafrac1 protein, Drosophila
  • Peroxidases
  • Thioredoxin Reductase 1
  • Glutathione