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J Biol Chem, Vol. 273, Issue 29, 18173-18179, July 17, 1998

Dissociation of GLUT4 Translocation and Insulin-stimulated Glucose Transport in Transgenic Mice Overexpressing GLUT1 in Skeletal Muscle

Polly A. HansenDagger , Weichen Wang§, Bess Adkins Marshallparallel , John O. HolloszyDagger , and Mike Mueckler§

From the Departments of Dagger  Medicine, § Cell Biology and Physiology, and parallel  Pediatrics, Washington University School of Medicine, St. Louis, Missouri 63110

Overexpression of the human GLUT1 glucose transporter protein in skeletal muscle of transgenic mice results in large increases in basal glucose transport and metabolism, but impaired stimulation of glucose transport by insulin, contractions, or hypoxia (Gulve, E. A., Ren, J.-M., Marshall, B. A., Gao, J., Hansen, P. A., Holloszy, J. O., and Mueckler, M. (1994) J. Biol. Chem. 269, 18366-18370). This study examined the relationship between glucose transport and cell-surface glucose transporter content in isolated skeletal muscle from wild-type and GLUT1-overexpressing mice using 2-deoxyglucose, 3-O-methylglucose, and the 2-N-[4-(1-azi-2,2,2-trifluoroethyl)benzoyl]-1,3-bis(D-mannos-4-yloxy)-2-propylamine exofacial photolabeling technique. Insulin (2 milliunits/ml) stimulated a 3-fold increase in 2-deoxyglucose uptake in extensor digitorum longus muscles of control mice (0.47 ± 0.07 µmol/ml/20 min in basal muscle versus 1.44 µmol/ml/20 min in insulin-stimulated muscle; mean ± S.E.). Insulin failed to increase 2-deoxyglucose uptake above basal rates in muscles overexpressing GLUT1 (4.00 ± 0.40 µmol/ml/20 min in basal muscle versus 3.96 ± 0.37 µmol/ml/20 min in insulin-stimulated muscle). A similar lack of insulin stimulation in muscles overexpressing GLUT1 was observed using 3-O-methylglucose. However, the magnitude of the insulin-stimulated increase in cell-surface GLUT4 photolabeling was nearly identical (~3-fold) in wild-type and GLUT1-overexpressing muscles. This apparently normal insulin-stimulated translocation of GLUT4 in GLUT1-overexpressing muscle was confirmed by immunoelectron microscopy. Our findings suggest that GLUT4 activity at the plasma membrane can be dissociated from the plasma membrane content of GLUT4 molecules and thus suggest that the intrinsic activity of GLUT4 is subject to regulation.

Copyright © 1998 by The American Society for Biochemistry and Molecular Biology, Inc.
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