Improved insulin sensitivity associated with reduced mitochondrial complex IV assembly and activity

FASEB J. 2013 Apr;27(4):1371-80. doi: 10.1096/fj.12-221879. Epub 2012 Dec 14.

Abstract

Mice lacking Surf1, a complex IV assembly protein, have ∼50-70% reduction in cytochrome c oxidase activity in all tissues yet a paradoxical increase in lifespan. Here we report that Surf1(-/-) mice have lower body (15%) and fat (20%) mass, in association with reduced lipid storage, smaller adipocytes, and elevated indicators of fatty acid oxidation in white adipose tissue (WAT) compared with control mice. The respiratory quotient in the Surf1(-/-) mice was significantly lower than in the control animals (0.83-0.93 vs. 0.90-0.98), consistent with enhanced fat utilization in Surf1(-/-) mice. Elevated fat utilization was associated with increased insulin sensitivity measured as insulin-stimulated glucose uptake, as well as an increase in insulin receptor levels (∼2-fold) and glucose transporter type 4 (GLUT4; ∼1.3-fold) levels in WAT in the Surf1(-/-) mice. The expression of peroxisome proliferator-activated receptor γ-coactivator 1-α (PGC-1α) mRNA and protein was up-regulated by 2.5- and 1.9-fold, respectively, in WAT from Surf1(-/-) mice, and the expression of PGC-1α target genes and markers of mitochondrial biogenesis was elevated. Together, these findings point to a novel and unexpected link between reduced mitochondrial complex IV activity, enhanced insulin sensitivity, and increased mitochondrial biogenesis that may contribute to the increased longevity in the Surf1(-/-) mice.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adipose Tissue, White / metabolism
  • Animals
  • Electron Transport Complex IV / genetics
  • Electron Transport Complex IV / metabolism*
  • Glucose Transporter Type 4 / genetics
  • Glucose Transporter Type 4 / metabolism
  • Insulin / metabolism
  • Insulin Resistance / genetics*
  • Male
  • Membrane Proteins / metabolism*
  • Mice
  • Mitochondria / genetics
  • Mitochondria / metabolism*
  • Mitochondrial Proteins / metabolism*
  • Muscle, Skeletal / metabolism
  • Oxidation-Reduction
  • PPAR gamma / metabolism
  • Receptor, Insulin / metabolism*

Substances

  • Glucose Transporter Type 4
  • Insulin
  • Membrane Proteins
  • Mitochondrial Proteins
  • PPAR gamma
  • Surf-1 protein
  • Electron Transport Complex IV
  • Receptor, Insulin