Glycinergic innervation of motoneurons is deficient in amyotrophic lateral sclerosis mice: a quantitative confocal analysis

Am J Pathol. 2009 Feb;174(2):574-85. doi: 10.2353/ajpath.2009.080557. Epub 2008 Dec 30.

Abstract

Altered motoneuron excitability is involved in amyotrophic lateral sclerosis pathobiology. To test the hypothesis that inhibitory interneuron innervation of spinal motoneurons is abnormal in an amyotrophic lateral sclerosis mouse model, we measured GABAergic, glycinergic, and cholinergic immunoreactive terminals on spinal motoneurons in mice expressing a mutant form of human superoxide dismutase-1 with a Gly93-->Ala substitution (G93A-SOD1) and in controls at different ages. Glutamic acid decarboxylase, glycine transporter-2, and choline acetyltransferase were used as markers for GABAergic, glycinergic, and cholinergic terminals, respectively. Triple immunofluorescent labeling of boutons contacting motoneurons was visualized by confocal microscopy and analyzed quantitatively. Glycine transporter-2-bouton density on lateral motoneurons was decreased significantly in G93A-SOD1 mice compared with controls. This reduction was absent at 6 weeks of age but present in asymptomatic 8-week-old mice and worsened with disease progression from 12 to 14 weeks of age. Motoneurons lost most glycinergic innervation by 16 weeks of age (end-stage) when there was a significant decrease in the numbers of motoneurons and choline acetyltransferase-positive boutons. No significant differences in glutamic acid decarboxylase-bouton densities were found in G93A-SOD1 mice. Reduction of glycinergic innervation preceded mitochondrial swelling and vacuolization. Calbindin-positive Renshaw cell number was decreased significantly at 12 weeks of age in G93A-SOD1 mice. Thus, either the selective loss of inhibitory glycinergic regulation of motoneuron function or glycinergic interneuron degeneration contributes to motoneuron degeneration in amyotrophic lateral sclerosis.

MeSH terms

  • Acetylcholine / metabolism
  • Amyotrophic Lateral Sclerosis / metabolism*
  • Amyotrophic Lateral Sclerosis / pathology
  • Animals
  • Choline O-Acetyltransferase / metabolism
  • Fluorescent Antibody Technique
  • Glutamate Decarboxylase / metabolism
  • Glycine / metabolism*
  • Glycine Plasma Membrane Transport Proteins / metabolism
  • Humans
  • Image Processing, Computer-Assisted
  • Male
  • Mice
  • Mice, Transgenic
  • Microscopy, Confocal
  • Motor Neurons / metabolism*
  • Neural Inhibition / physiology*
  • Presynaptic Terminals / metabolism*
  • Presynaptic Terminals / ultrastructure*
  • Superoxide Dismutase / genetics
  • Superoxide Dismutase-1
  • gamma-Aminobutyric Acid / metabolism

Substances

  • Glycine Plasma Membrane Transport Proteins
  • SOD1 protein, human
  • gamma-Aminobutyric Acid
  • Sod1 protein, mouse
  • Superoxide Dismutase
  • Superoxide Dismutase-1
  • Choline O-Acetyltransferase
  • Glutamate Decarboxylase
  • Acetylcholine
  • Glycine