Overexpression of PLIN5 in skeletal muscle promotes oxidative gene expression and intramyocellular lipid content without compromising insulin sensitivity

Biochim Biophys Acta. 2013 Apr;1831(4):844-52. doi: 10.1016/j.bbalip.2013.01.007. Epub 2013 Jan 22.

Abstract

Aims/hypothesis: While lipid deposition in the skeletal muscle is considered to be involved in obesity-associated insulin resistance, neutral intramyocellular lipid (IMCL) accumulation per se does not necessarily induce insulin resistance. We previously demonstrated that overexpression of the lipid droplet coat protein perilipin 2 augments intramyocellular lipid content while improving insulin sensitivity. Another member of the perilipin family, perilipin 5 (PLIN5), is predominantly expressed in oxidative tissues like the skeletal muscle. Here we investigated the effects of PLIN5 overexpression - in comparison with the effects of PLIN2 - on skeletal muscle lipid levels, gene expression profiles and insulin sensitivity.

Methods: Gene electroporation was used to overexpress PLIN5 in tibialis anterior muscle of rats fed a high fat diet. Eight days after electroporation, insulin-mediated glucose uptake in the skeletal muscle was measured by means of a hyperinsulinemic euglycemic clamp. Electron microscopy, fluorescence microscopy and lipid extractions were performed to investigate IMCL accumulation. Gene expression profiles were obtained using microarrays.

Results: TAG storage and lipid droplet size increased upon PLIN5 overexpression. Despite the higher IMCL content, insulin sensitivity was not impaired and DAG and acylcarnitine levels were unaffected. In contrast to the effects of PLIN2 overexpression, microarray data analysis revealed a gene expression profile favoring FA oxidation and improved mitochondrial function.

Conclusions/interpretation: Both PLIN2 and PLIN5 increase neutral IMCL content without impeding insulin-mediated glucose uptake. As opposed to the effects of PLIN2 overexpression, overexpression of PLIN5 in the skeletal muscle promoted expression of a cluster of genes under control of PPARα and PGC1α involved in FA catabolism and mitochondrial oxidation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Insulin / metabolism
  • Insulin Resistance / genetics
  • Insulin Resistance / physiology
  • Intracellular Signaling Peptides and Proteins / genetics
  • Intracellular Signaling Peptides and Proteins / metabolism*
  • Lipid Metabolism / genetics
  • Lipid Metabolism / physiology
  • Male
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • Muscle Proteins / genetics
  • Muscle Proteins / metabolism*
  • Muscle, Skeletal / metabolism*
  • Perilipin-2
  • Perilipin-5
  • Rats
  • Rats, Wistar
  • Triglycerides / metabolism

Substances

  • Insulin
  • Intracellular Signaling Peptides and Proteins
  • Membrane Proteins
  • Muscle Proteins
  • PLIN2 protein, human
  • PLIN5 protein, rat
  • Perilipin-2
  • Perilipin-5
  • Plin2 protein, rat
  • Triglycerides