Hepatic glycogen supercompensation activates AMP-activated protein kinase, impairs insulin signaling, and reduces glycogen deposition in the liver

Diabetes. 2011 Feb;60(2):398-407. doi: 10.2337/db10-0592.

Abstract

Objective: The objective of this study was to determine how increasing the hepatic glycogen content would affect the liver's ability to take up and metabolize glucose.

Research design and methods: During the first 4 h of the study, liver glycogen deposition was stimulated by intraportal fructose infusion in the presence of hyperglycemic-normoinsulinemia. This was followed by a 2-h hyperglycemic-normoinsulinemic control period, during which the fructose infusion was stopped, and a 2-h experimental period in which net hepatic glucose uptake (NHGU) and disposition (glycogen, lactate, and CO(2)) were measured in the absence of fructose but in the presence of a hyperglycemic-hyperinsulinemic challenge including portal vein glucose infusion.

Results: Fructose infusion increased net hepatic glycogen synthesis (0.7 ± 0.5 vs. 6.4 ± 0.4 mg/kg/min; P < 0.001), causing a large difference in hepatic glycogen content (62 ± 9 vs. 100 ± 3 mg/g; P < 0.001). Hepatic glycogen supercompensation (fructose infusion group) did not alter NHGU, but it reduced the percent of NHGU directed to glycogen (79 ± 4 vs. 55 ± 6; P < 0.01) and increased the percent directed to lactate (12 ± 3 vs. 29 ± 5; P = 0.01) and oxidation (9 ± 3 vs. 16 ± 3; P = NS). This change was associated with increased AMP-activated protein kinase phosphorylation, diminished insulin signaling, and a shift in glycogenic enzyme activity toward a state discouraging glycogen accumulation.

Conclusions: These data indicate that increases in hepatic glycogen can generate a state of hepatic insulin resistance, which is characterized by impaired glycogen synthesis despite preserved NHGU.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • AMP-Activated Protein Kinases / metabolism*
  • Analysis of Variance
  • Animals
  • Blood Glucose
  • Blotting, Western
  • Dogs
  • Fatty Acids, Nonesterified / blood
  • Female
  • Fructose / metabolism
  • Fructose / pharmacology
  • Glucagon / metabolism
  • Insulin / metabolism*
  • Liver / drug effects
  • Liver / metabolism*
  • Liver Glycogen / metabolism*
  • Male
  • Portal Vein / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Signal Transduction / physiology

Substances

  • Blood Glucose
  • Fatty Acids, Nonesterified
  • Insulin
  • Liver Glycogen
  • Fructose
  • Glucagon
  • AMP-Activated Protein Kinases