Exendin-4 ameliorates motor neuron degeneration in cellular and animal models of amyotrophic lateral sclerosis

PLoS One. 2012;7(2):e32008. doi: 10.1371/journal.pone.0032008. Epub 2012 Feb 23.

Abstract

Amyotrophic lateral sclerosis (ALS) is a devastating neurodegenerative disease characterized by a progressive loss of lower motor neurons in the spinal cord. The incretin hormone, glucagon-like peptide-1 (GLP-1), facilitates insulin signaling, and the long acting GLP-1 receptor agonist exendin-4 (Ex-4) is currently used as an anti-diabetic drug. GLP-1 receptors are widely expressed in the brain and spinal cord, and our prior studies have shown that Ex-4 is neuroprotective in several neurodegenerative disease rodent models, including stroke, Parkinson's disease and Alzheimer's disease. Here we hypothesized that Ex-4 may provide neuroprotective activity in ALS, and hence characterized Ex-4 actions in both cell culture (NSC-19 neuroblastoma cells) and in vivo (SOD1 G93A mutant mice) models of ALS. Ex-4 proved to be neurotrophic in NSC-19 cells, elevating choline acetyltransferase (ChAT) activity, as well as neuroprotective, protecting cells from hydrogen peroxide-induced oxidative stress and staurosporine-induced apoptosis. Additionally, in both wild-type SOD1 and mutant SOD1 (G37R) stably transfected NSC-19 cell lines, Ex-4 protected against trophic factor withdrawal-induced toxicity. To assess in vivo translation, SOD1 mutant mice were administered vehicle or Ex-4 at 6-weeks of age onwards to end-stage disease via subcutaneous osmotic pump to provide steady-state infusion. ALS mice treated with Ex-4 showed improved glucose tolerance and normalization of behavior, as assessed by running wheel, compared to control ALS mice. Furthermore, Ex-4 treatment attenuated neuronal cell death in the lumbar spinal cord; immunohistochemical analysis demonstrated the rescue of neuronal markers, such as ChAT, associated with motor neurons. Together, our results suggest that GLP-1 receptor agonists warrant further evaluation to assess whether their neuroprotective potential is of therapeutic relevance in ALS.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, N.I.H., Intramural

MeSH terms

  • Amyotrophic Lateral Sclerosis / metabolism*
  • Animals
  • Apoptosis
  • Cell Line
  • Choline O-Acetyltransferase / metabolism
  • Disease Models, Animal
  • Exenatide
  • Glucagon-Like Peptide 1 / antagonists & inhibitors
  • Glucagon-Like Peptide 1 / metabolism
  • Glucose Tolerance Test / methods
  • Hydrogen Peroxide / pharmacology
  • Hypoglycemic Agents / pharmacology
  • Insulin / metabolism
  • Male
  • Mice
  • Motor Neurons / metabolism*
  • Oxidative Stress
  • Peptides / pharmacology*
  • Spinal Cord / metabolism
  • Staurosporine / pharmacology
  • Superoxide Dismutase / metabolism
  • Superoxide Dismutase-1
  • Venoms / pharmacology*

Substances

  • Hypoglycemic Agents
  • Insulin
  • Peptides
  • Venoms
  • Glucagon-Like Peptide 1
  • Exenatide
  • Hydrogen Peroxide
  • Sod1 protein, mouse
  • Superoxide Dismutase
  • Superoxide Dismutase-1
  • Choline O-Acetyltransferase
  • Staurosporine