Counteracting neuronal nitric oxide synthase proteasomal degradation improves glucose transport in insulin-resistant skeletal muscle from Zucker fa/fa rats

Diabetologia. 2014 Jan;57(1):177-86. doi: 10.1007/s00125-013-3084-9. Epub 2013 Nov 2.

Abstract

Aims/hypothesis: Insulin-mediated glucose transport and utilisation are decreased in skeletal muscle from type 2 diabetic and glucose-intolerant individuals because of alterations in insulin receptor signalling, GLUT4 translocation to the plasma membrane and microvascular blood flow. Catalytic activity of the muscle-specific isoform of neuronal nitric oxide synthase (nNOS) also participates in the regulation of glucose transport and appears to be decreased in a relevant animal model of drastic insulin resistance, the obese Zucker fa/fa rat. Our objective was to determine the molecular mechanisms involved in this defect.

Methods: Isolated rat muscles and primary cultures of myocytes were used for western blot analysis of protein expression, immunohistochemistry, glucose uptake measurements and GLUT4 translocation assays.

Results: nNOS expression was reduced in skeletal muscle from fa/fa rats. This was caused by increased ubiquitination of the enzyme and subsequent degradation by the ubiquitin proteasome pathway. The degradation occurred through a greater interaction of nNOS with the chaperone heat-shock protein 70 and the co-chaperone, carboxyl terminus of Hsc70-interacting protein (CHIP). In addition, an alteration in nNOS sarcolemmal localisation was observed. We confirmed the implication of nNOS breakdown in defective insulin-induced glucose transport by demonstrating that blockade of proteasomal degradation or overexpression of nNOS improved basal and/or insulin-stimulated glucose uptake and GLUT4 translocation in primary cultures of insulin-resistant myocytes.

Conclusions/interpretation: Recovery of nNOS in insulin-resistant muscles should be considered a potential new approach to address insulin resistance.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Blotting, Western
  • Cells, Cultured
  • Glucose / metabolism*
  • Glucose Transporter Type 4 / metabolism
  • Immunoprecipitation
  • Insulin Resistance / physiology*
  • Male
  • Muscle Cells / metabolism
  • Muscle, Skeletal / metabolism*
  • Nitric Oxide Synthase Type I / genetics
  • Nitric Oxide Synthase Type I / metabolism*
  • Proteasome Endopeptidase Complex / metabolism*
  • Rats
  • Rats, Zucker
  • Reverse Transcriptase Polymerase Chain Reaction

Substances

  • Glucose Transporter Type 4
  • Nitric Oxide Synthase Type I
  • Proteasome Endopeptidase Complex
  • Glucose