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Am J Physiol Endocrinol Metab 274: E642-E650, 1998;
0193-1849/98 $5.00
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Vol. 274, Issue 4, E642-E650, April 1998

Time course of insulin action on tissue-specific intracellular glucose metabolism in normal rats

Sietse J. Koopmans, Lawrence Mandarino, and Ralph A. Defronzo

Department of Medicine, University of Texas Health Science Center and Audie L. Murphy Memorial Veterans Affairs Hospital, San Antonio, Texas 78284; and Department of Endocrinology and Metabolic Diseases, Leiden University Hospital, 2333 AA Leiden, The Netherlands

We investigated the time course of insulin action in conscious rats exposed to constant physiological hyperinsulinemia (~100 mU/l) while maintaining euglycemia (~100 mg/dl) for 0, 0.5, 2, 4, 8, or 12 h. [3-3H]glucose was infused to quantitate whole body glucose disposal (rate of disappearance, Rd), glycolysis (generation of 3H2O in plasma), hepatic glucose production (HGP), and skeletal muscle and liver glycogen synthesis ([3-3H]glucose incorporation into glycogen and time-dependent change in tissue glycogen concentration). The basal Rd, which equals HGP, was 6.0 ± 0.3 mg · kg-1 · min-1. With increased duration of hyperinsulinemia from 0 to 0.5 to 2 to 4 h, Rd increased from 6.0 ± 0.3 to 21.0 ± 1.1 to 24.1 ± 1.5 to 26.6 ± 0.6 mg · kg-1 · min-1 (P < 0.05 for 2 and 4 h vs. 0.5 h). During the first 2 h the increase in Rd was explained by parallel increases in glycolysis and glycogen synthesis. From 2 to 4 h the further increase in Rd was entirely due to an increase in glycolysis without change in glycogen synthesis. From 4 to 8 to 12 h of hyperinsulinemia, Rd decreased by 19% from 26.6 ± 0.6 to 24.1 ± 1.1 to 21.6 ± 1.8 mg · kg-1 · min-1 (P < 0.05 for 8 h vs. 4 h and 12 h vs. 8 h). The progressive decline in Rd, in the face of constant hyperinsulinemia, occurred despite a slight increase (8-14%) in glycolysis and was completely explained by a marked decrease (64%) in muscle glycogen synthesis. In contrast, liver glycogen synthesis increased fourfold, indicating an independent regulation of muscle and liver glycogen synthesis by long-term hyperinsulinemia. In the liver, during the entire 12-h period of insulin stimulation, the contribution of the direct (from glucose) and the indirect (from C-3 fragments) pathways to net glycogen formation remained constant at 77 ± 5 and 23 ± 5%, respectively. HGP remained suppressed throughout the 12-h period of hyperinsulinemia.

lipid metabolism; insulin resistance; glycogen synthesis; glycolysis; hepatic glucose production


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