Lack of myotubularin (MTM1) leads to muscle hypotrophy through unbalanced regulation of the autophagy and ubiquitin-proteasome pathways

FASEB J. 2013 Aug;27(8):3384-94. doi: 10.1096/fj.12-220947. Epub 2013 May 21.

Abstract

Mutations in the phosphoinositide phosphatase myotubularin (MTM1) results in X-linked myotubular/centronuclear myopathy (XLMTM), characterized by a severe decrease in muscle mass and strength in patients and murine models. However, the molecular mechanism involved in the muscle hypotrophy is unclear. Here we show that the IGF1R/Akt pathway is affected in Mtm1-deficient murine muscles, characterized by an increase in IGF1 receptor and Akt levels in both the presymptomatic and symptomatic phases. Moreover, up-regulation of atrogenes was observed in the presymptomatic phase of the myopathy, supporting overactivation of the ubiquitin-proteasome pathway. In parallel, the autophagy machinery was affected as indicated by the increase in the number of autophagosomes and of autophagy markers, such as LC3 and P62. However, phosphorylation of FOXO3a and mTOR were abnormal at late but not at early stages of the disease, suggesting that myotubularin acts both upstream in the IGF1R/Akt pathway and downstream on the balance between the autophagy and ubiquitin-proteasome pathways in vivo. Adeno-associated virus-mediated delivery of Mtm1 into Mtm1-null muscles rescued muscle mass and normalized the expression levels of IGF1 receptor, the ubiquitin-proteasome pathway, and autophagy markers. These data support the hypothesis that the unbalanced regulation of the ubiquitin proteasome pathway and the autophagy machinery is a primary cause of the XLMTM pathogenesis.

Keywords: atrogene; atrophy; centronuclear myopathy; myotubular myopathy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Autophagy*
  • Blotting, Western
  • Forkhead Box Protein O3
  • Forkhead Transcription Factors / metabolism
  • Gene Expression
  • Insulin-Like Growth Factor I / genetics
  • Insulin-Like Growth Factor I / metabolism
  • Male
  • Mice
  • Mice, 129 Strain
  • Mice, Knockout
  • Microscopy, Electron
  • Microtubule-Associated Proteins / genetics
  • Microtubule-Associated Proteins / metabolism
  • Muscle, Skeletal / metabolism
  • Muscle, Skeletal / pathology
  • Muscle, Skeletal / ultrastructure
  • Myopathies, Structural, Congenital / genetics
  • Myopathies, Structural, Congenital / metabolism*
  • Phosphorylation
  • Proteasome Endopeptidase Complex / metabolism*
  • Protein Tyrosine Phosphatases, Non-Receptor / deficiency*
  • Protein Tyrosine Phosphatases, Non-Receptor / genetics
  • Proto-Oncogene Proteins c-akt / genetics
  • Proto-Oncogene Proteins c-akt / metabolism
  • Receptor, IGF Type 1 / genetics
  • Receptor, IGF Type 1 / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Signal Transduction*
  • TOR Serine-Threonine Kinases / metabolism
  • Ubiquitin / metabolism*

Substances

  • Forkhead Box Protein O3
  • Forkhead Transcription Factors
  • FoxO3 protein, mouse
  • Map1lc3b protein, mouse
  • Microtubule-Associated Proteins
  • Ubiquitin
  • insulin-like growth factor-1, mouse
  • Insulin-Like Growth Factor I
  • mTOR protein, mouse
  • Receptor, IGF Type 1
  • Proto-Oncogene Proteins c-akt
  • TOR Serine-Threonine Kinases
  • Protein Tyrosine Phosphatases, Non-Receptor
  • myotubularin
  • Proteasome Endopeptidase Complex