ALS-Associated Endoplasmic Reticulum Proteins in Denervated Skeletal Muscle: Implications for Motor Neuron Disease Pathology

Brain Pathol. 2017 Nov;27(6):781-794. doi: 10.1111/bpa.12453. Epub 2017 Feb 15.

Abstract

Alpha-motoneurons and muscle fibres are structurally and functionally interdependent. Both cell types particularly rely on endoplasmic reticulum (ER/SR) functions. Mutations of the ER proteins VAPB, SigR1 and HSP27 lead to hereditary motor neuron diseases (MNDs). Here, we determined the expression profile and localization of these ER proteins/chaperons by immunohistochemistry and immunoblotting in biopsy and autopsy muscle tissue of patients with amyotrophic lateral sclerosis (ALS) and other neurogenic muscular atrophies (NMAs) and compared these patterns to mouse models of neurogenic muscular atrophy. Postsynaptic neuromuscular junction staining for VAPB was intense in normal human and mouse muscle and decreased in denervated Nmd2J mouse muscle fibres. In contrast, VAPB levels together with other chaperones and autophagy markers were increased in extrasynaptic regions of denervated muscle fibres of patients with MNDs and other NMAs, especially at sites of focal myofibrillar disintegration (targets). These findings did not differ between NMAs due to ALS and other causes. G93A-SOD1 mouse muscle fibres showed a similar pattern of protein level increases in denervated muscle fibres. In addition, they showed globular VAPB-immunoreactive structures together with misfolded SOD1 protein accumulations, suggesting a primary myopathic change. Our findings indicate that altered expression and localization of these ER proteins and autophagy markers are part of the dynamic response of muscle fibres to denervation. The ER is particularly prominent and vulnerable in both muscle fibres and alpha-motoneurons. Thus, ER pathology could contribute to the selective build-up of degenerative changes in the neuromuscular axis in MNDs.

Keywords: ALS; ER chaperones; Motor neuron disease (MND); Neurogenic muscular atrophy (NMA); Neuromuscular junction (NMJ); Sigma Receptor 1 (SigR1); VAPB.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amyotrophic Lateral Sclerosis / physiopathology
  • Animals
  • Autopsy
  • Disease Models, Animal
  • Endoplasmic Reticulum / pathology
  • Humans
  • Immunohistochemistry
  • Membrane Proteins / metabolism*
  • Membrane Proteins / physiology*
  • Mice
  • Mice, Transgenic
  • Motor Neuron Disease / pathology*
  • Motor Neurons / metabolism
  • Muscle Denervation
  • Muscle, Skeletal / pathology
  • Neuromuscular Junction
  • Spinal Cord / pathology
  • Superoxide Dismutase / metabolism
  • Superoxide Dismutase-1 / metabolism
  • Vesicular Transport Proteins / physiology

Substances

  • Membrane Proteins
  • VAPB protein, human
  • VAPB protein, mouse
  • Vesicular Transport Proteins
  • Superoxide Dismutase
  • Superoxide Dismutase-1