Expression of a Mutant SEMA3A Protein with Diminished Signalling Capacity Does Not Alter ALS-Related Motor Decline, or Confer Changes in NMJ Plasticity after BotoxA-Induced Paralysis of Male Gastrocnemic Muscle

PLoS One. 2017 Jan 19;12(1):e0170314. doi: 10.1371/journal.pone.0170314. eCollection 2017.

Abstract

Terminal Schwann cells (TSCs) are specialized cells that envelop the motor nerve terminal, and play a role in the maintenance and regeneration of neuromuscular junctions (NMJs). The chemorepulsive protein semaphorin 3A (SEMA3A) is selectively up-regulated in TSCs on fast-fatigable muscle fibers following experimental denervation of the muscle (BotoxA-induced paralysis or crush injury to the sciatic nerve) or in the motor neuron disease amyotrophic lateral sclerosis (ALS). Re-expression of SEMA3A in this subset of TSCs is thought to play a role in the selective plasticity of nerve terminals as observed in ALS and following BotoxA-induced paralysis. Using a mouse model expressing a mutant SEMA3A with diminished signaling capacity, we studied the influence of SEMA3A signaling at the NMJ with two denervation paradigms; a motor neuron disease model (the G93A-hSOD1 ALS mouse line) and an injury model (BotoxA-induced paralysis). ALS mice that either expressed 1 or 2 mutant SEMA3A alleles demonstrated no difference in ALS-induced decline in motor behavior. We also investigated the effects of BotoxA-induced paralysis on the sprouting capacity of NMJs in the K108N-SEMA3A mutant mouse, and observed no change in the differential neuronal plasticity found at NMJs on fast-fatigable or slow muscle fibers due to the presence of the SEMA3A mutant protein. Our data may be explained by the residual repulsive activity of the mutant SEMA3A, or it may imply that SEMA3A alone is not a key component of the molecular signature affecting NMJ plasticity in ALS or BotoxA-induced paralysis. Interestingly, we did observe a sex difference in motor neuron sprouting behavior after BotoxA-induced paralysis in WT mice which we speculate may be an important factor in the sex dimorphic differences seen in ALS.

MeSH terms

  • Amino Acid Substitution
  • Amyotrophic Lateral Sclerosis / genetics*
  • Amyotrophic Lateral Sclerosis / pathology
  • Amyotrophic Lateral Sclerosis / physiopathology
  • Animals
  • Botulinum Toxins, Type A / toxicity
  • Denervation
  • Disease Models, Animal
  • Female
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Mutant Strains
  • Mice, Transgenic
  • Motor Neurons / drug effects
  • Motor Neurons / pathology
  • Motor Neurons / physiology
  • Mutant Proteins / genetics
  • Mutant Proteins / metabolism
  • Neuromuscular Junction / drug effects
  • Neuromuscular Junction / genetics*
  • Neuromuscular Junction / physiology
  • Neuronal Plasticity / drug effects
  • Neuronal Plasticity / genetics
  • Neuronal Plasticity / physiology
  • Paralysis / chemically induced
  • Paralysis / genetics*
  • Paralysis / physiopathology
  • Schwann Cells / physiology
  • Semaphorin-3A / genetics*
  • Semaphorin-3A / metabolism*
  • Signal Transduction

Substances

  • Mutant Proteins
  • Sema3a protein, mouse
  • Semaphorin-3A
  • Botulinum Toxins, Type A

Grants and funding

This work was supported by EU Seventh Framework Program (FP7) Marie Curie Actions (AxRegen) 2008-2012 to JV. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.