Sarcolipin deletion exacerbates soleus muscle atrophy and weakness in phospholamban overexpressing mice

PLoS One. 2017 Mar 9;12(3):e0173708. doi: 10.1371/journal.pone.0173708. eCollection 2017.

Abstract

Sarcolipin (SLN) and phospholamban (PLN) are two small proteins that regulate the sarco(endo)plasmic reticulum Ca2+-ATPase pumps. In a recent study, we discovered that Pln overexpression (PlnOE) in slow-twitch type I skeletal muscle fibers drastically impaired SERCA function and caused a centronuclear myopathy-like phenotype, severe muscle atrophy and weakness, and an 8 to 9-fold upregulation of SLN protein in the soleus muscles. Here, we sought to determine the physiological role of SLN upregulation, and based on its role as a SERCA inhibitor, we hypothesized that it would represent a maladaptive response that contributes to the SERCA dysfunction and the overall myopathy observed in the PlnOE mice. To this end, we crossed Sln-null (SlnKO) mice with PlnOE mice to generate a PlnOE/SlnKO mouse colony and assessed SERCA function, CNM pathology, in vitro contractility, muscle mass, calcineurin signaling, daily activity and food intake, and proteolytic enzyme activity. Our results indicate that genetic deletion of Sln did not improve SERCA function nor rescue the CNM phenotype, but did result in exacerbated muscle atrophy and weakness, due to a failure to induce type II fiber compensatory hypertrophy and a reduction in total myofiber count. Mechanistically, our findings suggest that impaired calcineurin activation and resultant decreased expression of stabilin-2, and/or impaired autophagic signaling could be involved. Future studies should examine these possibilities. In conclusion, our study demonstrates the importance of SLN upregulation in combating muscle myopathy in the PlnOE mice, and since SLN is upregulated across several myopathies, our findings may reveal SLN as a novel and universal therapeutic target.

MeSH terms

  • Animals
  • Calcium / metabolism
  • Calcium-Binding Proteins / physiology*
  • Disease Models, Animal
  • Female
  • Ion Transport
  • Male
  • Mice
  • Mice, Knockout
  • Muscle Contraction
  • Muscle Fibers, Slow-Twitch / metabolism
  • Muscle Fibers, Slow-Twitch / pathology*
  • Muscle Proteins / physiology*
  • Muscle, Skeletal / metabolism
  • Muscle, Skeletal / pathology*
  • Muscular Atrophy / metabolism
  • Muscular Atrophy / pathology*
  • Proteolipids / physiology*
  • Sarcoplasmic Reticulum / metabolism
  • Sarcoplasmic Reticulum / pathology*
  • Sarcoplasmic Reticulum Calcium-Transporting ATPases / metabolism*
  • Sequence Deletion

Substances

  • Calcium-Binding Proteins
  • Muscle Proteins
  • Proteolipids
  • phospholamban
  • sarcolipin
  • Sarcoplasmic Reticulum Calcium-Transporting ATPases
  • Calcium

Grants and funding

This work was supported by research grants from the Canadian Institutes of Health Research (MOP 86618 and MOP 47296 to A.R.T). A doctoral award from the Canadian Institutes of Health Research supported V.A.F. and doctoral awards from the Natural Sciences and Engineering Research Council supported A.M. and D.B.