Muscle mitochondrial ATP synthesis and glucose transport/phosphorylation in type 2 diabetes

PLoS Med. 2007 May;4(5):e154. doi: 10.1371/journal.pmed.0040154.

Abstract

Background: Muscular insulin resistance is frequently characterized by blunted increases in glucose-6-phosphate (G-6-P) reflecting impaired glucose transport/phosphorylation. These abnormalities likely relate to excessive intramyocellular lipids and mitochondrial dysfunction. We hypothesized that alterations in insulin action and mitochondrial function should be present even in nonobese patients with well-controlled type 2 diabetes mellitus (T2DM).

Methods and findings: We measured G-6-P, ATP synthetic flux (i.e., synthesis) and lipid contents of skeletal muscle with (31)P/(1)H magnetic resonance spectroscopy in ten patients with T2DM and in two control groups: ten sex-, age-, and body mass-matched elderly people; and 11 younger healthy individuals. Although insulin sensitivity was lower in patients with T2DM, muscle lipid contents were comparable and hyperinsulinemia increased G-6-P by 50% (95% confidence interval [CI] 39%-99%) in all groups. Patients with diabetes had 27% lower fasting ATP synthetic flux compared to younger controls (p = 0.031). Insulin stimulation increased ATP synthetic flux only in controls (younger: 26%, 95% CI 13%-42%; older: 11%, 95% CI 2%-25%), but failed to increase even during hyperglycemic hyperinsulinemia in patients with T2DM. Fasting free fatty acids and waist-to-hip ratios explained 44% of basal ATP synthetic flux. Insulin sensitivity explained 30% of insulin-stimulated ATP synthetic flux.

Conclusions: Patients with well-controlled T2DM feature slightly lower flux through muscle ATP synthesis, which occurs independently of glucose transport /phosphorylation and lipid deposition but is determined by lipid availability and insulin sensitivity. Furthermore, the reduction in insulin-stimulated glucose disposal despite normal glucose transport/phosphorylation suggests further abnormalities mainly in glycogen synthesis in these patients.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate / biosynthesis*
  • Adipose Tissue / metabolism
  • Adipose Tissue / physiology
  • Adult
  • Aged
  • Blood Glucose / metabolism*
  • Diabetes Mellitus, Type 2 / metabolism*
  • Fatty Acids, Nonesterified / metabolism
  • Female
  • Glucose Clamp Technique
  • Glucose-6-Phosphate / blood
  • Humans
  • Insulin Resistance / physiology*
  • Magnetic Resonance Spectroscopy
  • Male
  • Middle Aged
  • Mitochondria, Muscle / metabolism*
  • Obesity / metabolism
  • Obesity / physiopathology
  • Phosphorylation

Substances

  • Blood Glucose
  • Fatty Acids, Nonesterified
  • Glucose-6-Phosphate
  • Adenosine Triphosphate