Alternative splicing dysregulation secondary to skeletal muscle regeneration

Ann Neurol. 2011 Apr;69(4):681-90. doi: 10.1002/ana.22278. Epub 2011 Mar 11.

Abstract

Objective: Dysregulation of alternative splicing has become a molecular hallmark of myotonic dystrophy type 1 (DM1), in which neonatal splice variants are expressed in adult skeletal muscle. Splicing dysregulation is induced by RNA containing expanded CUG repeats expressed from the expanded mutant allele by sequestration of muscleblindlike 1 (MBNL1) protein within nuclear RNA foci and increased CUGBP, ELAV-like family member 1 (CELF1) protein levels. Dysregulated splicing has also been identified in other neuromuscular disorders, suggesting either that diseases with different molecular causes share a common pathogenic mechanism or that dysregulated splicing can also be a common secondary consequence of muscle degeneration and regeneration.

Methods: In this study, we examined regulation of alternative splicing in 4 different mouse models of muscular dystrophy, including DM1, limb-girdle muscular dystrophy, congenital merosin-deficient muscular dystrophy, and Duchenne muscular dystrophy, and 2 myotoxin (cardiotoxin and notexin) muscle injury models.

Results: We show that DM1-like alternative splicing dysregulation and altered expression of MBNL1 and CELF1 occur in non-DM1 mouse models of muscular dystrophy and muscle injury, most likely due to recapitulation of neonatal splicing patterns in regenerating fibers. In contrast, CELF1 was elevated in nuclei of mature myofibers of the DM1 model, consistent with a primary effect of pathogenic RNA expression.

Interpretation: Splicing dysregulation in DM1 is a primary effect of RNA containing expanded CUG repeats. However, we conclude that splicing changes can also be observed secondary to muscle regeneration, and this possibility must be taken into account when evaluating cause-effect relationships between dysregulated splicing and disease processes.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alternative Splicing*
  • Animals
  • Animals, Newborn
  • Blotting, Western
  • Cardiotoxins / adverse effects
  • Disease Models, Animal
  • Elapid Venoms / adverse effects
  • Fluorescent Antibody Technique
  • In Situ Hybridization, Fluorescence
  • Mice
  • Mice, Inbred C57BL
  • Mice, Inbred Strains
  • Mice, Inbred mdx
  • Muscle, Skeletal / drug effects
  • Muscle, Skeletal / metabolism
  • Muscle, Skeletal / physiopathology*
  • Muscular Dystrophies / genetics
  • Muscular Dystrophies / metabolism*
  • Muscular Dystrophies, Limb-Girdle / metabolism
  • Muscular Dystrophy, Duchenne / metabolism
  • Myotonic Dystrophy / metabolism
  • RNA-Binding Proteins / metabolism
  • Regeneration*
  • Reverse Transcriptase Polymerase Chain Reaction
  • Up-Regulation

Substances

  • Cardiotoxins
  • Elapid Venoms
  • RNA-Binding Proteins
  • notexin

Supplementary concepts

  • Muscular dystrophy congenital, merosin negative