Early interneuron dysfunction in ALS: insights from a mutant sod1 zebrafish model

Ann Neurol. 2013 Feb;73(2):246-58. doi: 10.1002/ana.23780. Epub 2012 Dec 31.

Abstract

Objective: To determine, when, how, and which neurons initiate the onset of pathophysiology in amyotrophic lateral sclerosis (ALS) using a transgenic mutant sod1 zebrafish model and identify neuroprotective drugs.

Methods: Proteinopathies such as ALS involve mutant proteins that misfold and activate the heat shock stress response (HSR). The HSR is indicative of neuronal stress, and we used a fluorescent hsp70-DsRed reporter in our transgenic zebrafish to track neuronal stress and to measure functional changes in neurons and muscle over the course of the disease.

Results: We show that mutant sod1 fish first exhibited the HSR in glycinergic interneurons at 24 hours postfertilization (hpf). By 96 hpf, we observed a significant reduction in spontaneous glycinergic currents induced in spinal motor neurons. The loss of inhibition was followed by increased stress in the motor neurons of symptomatic adults and concurrent morphological changes at the neuromuscular junction (NMJ) indicative of denervation. Riluzole, the only approved ALS drug and apomorphine, an NRF2 activator, reduced the observed early neuronal stress response.

Interpretation: The earliest event in the pathophysiology of ALS in the mutant sod1 zebrafish model involves neuronal stress in inhibitory interneurons, resulting from mutant Sod1 expression. This is followed by a reduction in inhibitory input to motor neurons. The loss of inhibitory input may contribute to the later development of neuronal stress in motor neurons and concurrent inability to maintain the NMJ. Riluzole, the approved drug for use in ALS, modulates neuronal stress in interneurons, indicating a novel mechanism of riluzole action.

Publication types

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

MeSH terms

  • Amyotrophic Lateral Sclerosis / drug therapy
  • Amyotrophic Lateral Sclerosis / genetics
  • Amyotrophic Lateral Sclerosis / pathology
  • Amyotrophic Lateral Sclerosis / physiopathology*
  • Animals
  • Animals, Genetically Modified
  • Apomorphine / pharmacology
  • Disease Models, Animal*
  • Dopamine Agonists / pharmacology
  • Genes, Reporter
  • Glycine / physiology
  • HSP72 Heat-Shock Proteins / genetics
  • Humans
  • Interneurons / drug effects
  • Interneurons / pathology
  • Interneurons / physiology*
  • Mice
  • Motor Neurons / drug effects
  • Motor Neurons / pathology
  • Motor Neurons / physiology
  • Muscle, Skeletal / innervation
  • NF-E2-Related Factor 2 / metabolism
  • Neuromuscular Junction / pathology
  • Neuromuscular Junction / physiopathology
  • Neuroprotective Agents
  • Patch-Clamp Techniques
  • Riluzole / pharmacology
  • Stress, Physiological / drug effects
  • Stress, Physiological / physiology
  • Superoxide Dismutase / genetics*
  • Superoxide Dismutase / metabolism
  • Superoxide Dismutase-1
  • Zebrafish Proteins / metabolism
  • Zebrafish*

Substances

  • Dopamine Agonists
  • HSP72 Heat-Shock Proteins
  • NF-E2-Related Factor 2
  • Neuroprotective Agents
  • SOD1 protein, human
  • Zebrafish Proteins
  • nfe2l2a protein, zebrafish
  • Riluzole
  • Sod1 protein, mouse
  • Superoxide Dismutase
  • Superoxide Dismutase-1
  • Apomorphine
  • Glycine