Early differences in membrane properties at the neuromuscular junctions of ALS model mice: Effects of 25-hydroxycholesterol

Life Sci. 2021 May 15:273:119300. doi: 10.1016/j.lfs.2021.119300. Epub 2021 Mar 2.

Abstract

Aims: Plasma hyperlipidemia is a protective factor in amyotrophic lateral sclerosis (ALS) while cholesterol-lowering drugs aggravate the pathology. We hypothesize that this phenomenon can be linked with membrane lipid alterations in the neuromuscular junctions (NMJs) occurring before motor neuron loss.

Methods: Neurotransmitter release in parallel with lipid membrane properties in diaphragm NMJs of SOD1G93A (mSOD) mice at nine weeks of age (pre-onset stage) were assessed.

Key findings: Despite on slight changes in spontaneous and evoked quantum release of acetylcholine, extracellular levels of choline at resting conditions, an indicator of non-quantum release, were significantly increased in mSOD mice. The use of lipid-sensitive fluorescent probes points to lipid raft disruption in the NMJs of mSOD mice. However, content of cholesterol, a key raft component was unchanged implying another pathway responsible for the loss of raft integrity. In the mSOD mice we found marked increase in levels of raft-destabilizing lipid ceramide. This was accompanied by enhanced ability to uptake of exogenous ceramide in NMJs. Acute and chronic administration of 25-hydroxycholesterol, whose levels increase due to hypercholesterolemia, recovered early alterations in membrane properties. Furthermore, chronic treatment with 25-hydroxycholesterol prevented increase in ceramide and extracellular choline levels as well as suppressed lipid peroxidation of NMJ membranes and fragmentation of end plates.

Significance: Thus, lipid raft disruption likely due to ceramide accumulation could be early event in ALS which may trigger neuromuscular abnormalities. Cholesterol derivative 25-hydroxycholesterol may serve as a molecule restoring the membrane and functional properties of NMJs at the early stage.

Keywords: 25-Hydroxycholesterol; Amyotrophic lateral sclerosis; Ceramide; Lipid rafts; Neuromuscular junction; Reactive oxygen species.

MeSH terms

  • Acetylcholine / metabolism
  • Amyotrophic Lateral Sclerosis / drug therapy*
  • Amyotrophic Lateral Sclerosis / metabolism
  • Amyotrophic Lateral Sclerosis / pathology
  • Animals
  • Ceramides / metabolism
  • Cholesterol / metabolism
  • Disease Models, Animal*
  • Female
  • Hydroxycholesterols / pharmacology*
  • Male
  • Membrane Microdomains / drug effects*
  • Membrane Microdomains / metabolism
  • Membrane Microdomains / pathology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Muscle, Skeletal / drug effects*
  • Muscle, Skeletal / metabolism
  • Muscle, Skeletal / pathology
  • Neuromuscular Junction
  • Superoxide Dismutase-1 / physiology*
  • Synaptic Transmission

Substances

  • Ceramides
  • Hydroxycholesterols
  • 25-hydroxycholesterol
  • Cholesterol
  • Sod1 protein, mouse
  • Superoxide Dismutase-1
  • Acetylcholine