Polyethylene glycol-coupled IGF1 delays motor function defects in a mouse model of spinal muscular atrophy with respiratory distress type 1

Brain. 2014 May;137(Pt 5):1374-93. doi: 10.1093/brain/awu059. Epub 2014 Mar 27.

Abstract

Spinal muscular atrophy with respiratory distress type 1 is a neuromuscular disorder characterized by progressive weakness and atrophy of the diaphragm and skeletal muscles, leading to death in childhood. No effective treatment is available. The neuromuscular degeneration (Nmd(2J)) mouse shares a crucial mutation in the immunoglobulin mu-binding protein 2 gene (Ighmbp2) with spinal muscular atrophy with respiratory distress type 1 patients and also displays some basic features of the human disease. This model serves as a promising tool in understanding the complex mechanisms of the disease and in exploring novel treatment modalities such as insulin-like growth factor 1 (IGF1) which supports myogenic and neurogenic survival and stimulates differentiation during development. Here we investigated the treatment effects with polyethylene glycol-coupled IGF1 and its mechanisms of action in neurons and muscles. Polyethylene glycol-coupled IGF1 was applied subcutaneously every second day from post-natal Day 14 to post-natal Day 42 and the outcome was assessed by morphology, electromyography, and molecular studies. We found reduced IGF1 serum levels in Nmd(2J) mice 2 weeks after birth, which was normalized by polyethylene glycol-coupled IGF1 treatment. Nmd(2J) mice showed marked neurogenic muscle fibre atrophy in the gastrocnemius muscle and polyethylene glycol-coupled IGF1 treatment resulted in muscle fibre hypertrophy and slowed fibre degeneration along with significantly higher numbers of functionally active axonal sprouts. In the diaphragm with predominant myogenic changes a profound protection from muscle fibre degeneration was observed under treatment. No effects of polyethylene glycol-coupled IGF1 were monitored at the level of motor neuron survival. The beneficial effects of polyethylene glycol-coupled IGF1 corresponded to a marked activation of the IGF1 receptor, resulting in enhanced phosphorylation of Akt (protein kinase B) and the ribosomal protein S6 kinase in striated muscles and spinal cord from Nmd(2J) mice. Based on these findings, polyethylene glycol-coupled IGF1 may hold promise as a candidate for future treatment trials in human patients with spinal muscular atrophy with respiratory distress type 1.

Keywords: Akt/p70S6K; DSMA1; Nmd2J mouse; PEG-IGF1; SMARD1.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Age Factors
  • Animals
  • Cells, Cultured
  • Ciliary Neurotrophic Factor / pharmacology
  • DNA-Binding Proteins / genetics
  • Disease Models, Animal
  • Gene Expression Regulation / drug effects
  • Gene Expression Regulation / genetics
  • Insulin-Like Growth Factor I / metabolism
  • Insulin-Like Growth Factor I / pharmacology
  • Insulin-Like Growth Factor I / therapeutic use*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Movement Disorders / drug therapy*
  • Movement Disorders / etiology*
  • Muscle Strength / drug effects
  • Muscle Strength / genetics
  • Muscle, Skeletal / drug effects
  • Muscle, Skeletal / physiopathology
  • Muscular Atrophy, Spinal / complications*
  • Muscular Atrophy, Spinal / genetics
  • Muscular Atrophy, Spinal / therapy
  • Myocardium / pathology
  • Polyethylene Glycols / therapeutic use*
  • Receptor, IGF Type 1 / metabolism
  • Time Factors
  • Transcription Factors / genetics

Substances

  • Ciliary Neurotrophic Factor
  • DNA-Binding Proteins
  • Ighmbp2 protein, mouse
  • Transcription Factors
  • Polyethylene Glycols
  • Insulin-Like Growth Factor I
  • Receptor, IGF Type 1