Dysfunctional muscle and liver glycogen metabolism in mdx dystrophic mice

PLoS One. 2014 Mar 13;9(3):e91514. doi: 10.1371/journal.pone.0091514. eCollection 2014.

Abstract

Background: Duchenne muscular dystrophy (DMD) is a severe, genetic muscle wasting disorder characterised by progressive muscle weakness. DMD is caused by mutations in the dystrophin (dmd) gene resulting in very low levels or a complete absence of the dystrophin protein, a key structural element of muscle fibres which is responsible for the proper transmission of force. In the absence of dystrophin, muscle fibres become damaged easily during contraction resulting in their degeneration. DMD patients and mdx mice (an animal model of DMD) exhibit altered metabolic disturbances that cannot be attributed to the loss of dystrophin directly. We tested the hypothesis that glycogen metabolism is defective in mdx dystrophic mice.

Results: Dystrophic mdx mice had increased skeletal muscle glycogen (79%, (P<0.01)). Skeletal muscle glycogen synthesis is initiated by glycogenin, the expression of which was increased by 50% in mdx mice (P<0.0001). Glycogen synthase activity was 12% higher (P<0.05) but glycogen branching enzyme activity was 70% lower (P<0.01) in mdx compared with wild-type mice. The rate-limiting enzyme for glycogen breakdown, glycogen phosphorylase, had 62% lower activity (P<0.01) in mdx mice resulting from a 24% reduction in PKA activity (P<0.01). In mdx mice glycogen debranching enzyme expression was 50% higher (P<0.001) together with starch-binding domain protein 1 (219% higher; P<0.01). In addition, mdx mice were glucose intolerant (P<0.01) and had 30% less liver glycogen (P<0.05) compared with control mice. Subsequent analysis of the enzymes dysregulated in skeletal muscle glycogen metabolism in mdx mice identified reduced glycogenin protein expression (46% less; P<0.05) as a possible cause of this phenotype.

Conclusion: We identified that mdx mice were glucose intolerant, and had increased skeletal muscle glycogen but reduced amounts of liver glycogen.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cyclic AMP-Dependent Protein Kinases / metabolism
  • Disease Models, Animal
  • Dystrophin / physiology
  • Glucose Intolerance
  • Glycogen / metabolism*
  • Glycogen Phosphorylase / metabolism
  • Liver / metabolism*
  • Liver / physiopathology*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Inbred mdx
  • Mice, Transgenic
  • Muscle, Skeletal / metabolism*
  • Muscle, Skeletal / physiopathology*
  • Phenotype

Substances

  • Dystrophin
  • Glycogen
  • Glycogen Phosphorylase
  • Cyclic AMP-Dependent Protein Kinases

Grants and funding

Supported by the Muscular Dystrophy Association (project grant 175821 to Gordon S. Lynch). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.