Evidence for defects in the trafficking and translocation of GLUT4 glucose transporters in skeletal muscle as a cause of human insulin resistance

Journal of Clinical Investigation

Volumn 101, Issue 11, 1998, Pages 2377-2386

  Garvey, W Timothy ^a,c   Maianu, Lidia ^a   Zhu, Ju Hong ^a   Brechtel Hook, Ginger ^b   Wallace, Penny ^a   Baron, Alain D ^b  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

GLUT4; Insulin resistance; Insulin regulated aminopeptidase (vp165); Type 2 diabetes mellitus; Vesicle trafficking

Indexed keywords

GLUCOSE TRANSPORTER; INSULIN;

ADIPOCYTE; ADULT; ARTICLE; CELL FRACTIONATION; CELLULAR DISTRIBUTION; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; GLUCOSE TRANSPORT SYSTEM; HUMAN; INSULIN RESISTANCE; MALE; MEMBRANE VESICLE; MUSCLE FIBER MEMBRANE; NON INSULIN DEPENDENT DIABETES MELLITUS; PRIORITY JOURNAL; SARCOLEMMA; SKELETAL MUSCLE;

EID: 0032104120     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI1557     Document Type: Article

References (56)

1. Reaven, G.M. 1995. Pathophysiology of insulin resistance in human disease. Physiol. Rev. 75:473-486.
2. Warram, J.H., B.C. Martin, A.S. Krolewski, J.S. Soeldner, and C.R. Kahn. 1990. Slow glucose removal rate and hyperinsulinemia precede the development of type II diabetes in the offspring of diabetic parents. Ann. Intern. Med. 113:909-915.
3. DeFronzo, R.A., E. Jacot, E. Jequier, E. Maeder, and J.P. Felber. 1981. The effect of insulin on the disposal of intravenous glucose: results from indirect calorimetry and hepatic and femoral venous catheterization. Diabetes. 30: 1000-1007.
4. Garvey, W.T., and M. Birnbaum. 1993. Cellular insulin action and insulin resistance. In Bailliere's clinical endocrinology and metabolism: insulin resistance and disease. E. Ferrannini, editor. Bailliere Tindall, London. 785-873.
5. Bonadonna, R.C., S. Del Prato, M.P. Sacomani, E. Bonora, G. Gulli, E. Ferrannini, D. Bier, C. Cobelli, and R.A. DeFronzo. 1993. Transmembrane glucose transport in skeletal muscle of patients with non-insulin-dependent diabetes. J. Clin. Invest. 92:486-494.
6. Kelley, D.E., M.A. Minton, S.C. Watkins, J.-A. Simoneau, F. Jadali, A. Fredrickson, J. Beattie, and R. Theriault. 1996. The effect of non-insulin-dependent diabetes mellitus and obesity on glucose transport and phosphorylation in skeletal muscle. J. Clin. Invest. 97:2705-2713.
7. Katz, A., B.L. Nyomba, and C. Bogardus. 1988. No accumulation of glucose in human skeletal muscle during euglycemic hyperinsulinemia. Am. J. Physiol. 255:E942-E945.
8. Ziel, F.H., N. Venkatesan, and M.B. Davidson. 1988. Glucose transport is rate limiting for skeletal muscle glucose metabolism in normal and STZ-induced diabetic rats. Diabetes. 37:885-890.
9. 13C nuclear magnetic resonance spectroscopy. N. Engl. J. Med. 322:223-228.
10. Butler, P.C., E.J. Kryshak, M. Marsh, and R.A. Rizza. 1990. Effect of insulin on oxidation of intracellularly and extracellularly derived glucose in patients with NIDDM: evidence for primary defect in glucose transport and/or phosphorylation but not oxidation. Diabetes. 39:1371-1380.
11. Kelley, D.E., J.P. Reilly, T. Veneman, and L.J. Mandarino. 1990. Effects of insulin on skeletal muscle glucose storage, oxidation, and glycolysis in humans. Am. J. Physiol. 258:E923-E929.
12. Henry, R.R., B. Gumbiner, T. Flynn, and A.W. Thorburn. 1990. Metabolic effects of hyperglycemia and hyperinsulinemia on fate of intracellular glucose in NIDDM. Diabetes. 39:149-156.
13. Dohm, G.L., E.B. Tapscott, W.J. Pories, D.J. Dabbs, E.G. Flickinger, D. Meelheim, T. Fushiki, S.M. Atkinson, C.W. Elton, and J.F. Caro. 1988. An in vitro human muscle preparation suitable for metabolic studies: decreased insulin stimulation of glucose transport in muscle from morbidly obese and diabetic subjects. J. Clin. Invest. 82:486-494.
14. Andreasson, K., D. Galuska, A. Thorne, T. Sonnenfeld, and H. Wallberg-Henriksson. 1991. Decreased insulin-stimulated 3-O-mcthylglucose transport in vitro incubated muscle strips from type II diabetic subjects. Acta. Physiol. Scand. 142:255-260.
15. Garvey, W.T., L. Maianu, T.P. Huecksteadt, M.J. Birnbaum, M.J. Molina, and T.P. Ciaraldi. 1991. Pretranslational suppression of a glucose transporter protein causes cellular insulin resistance in non-insulin-dependent diabetes mellitus and obesity. J. Clin. Invest. 87:1072-1081.
16. Garvey, W.T., L. Maianu, J.-H. Zhu, J.A. Hancock, and A.M. Golichowski. 1993. Multiple defects in the adipocyte glucose transport system cause cellular insulin resistance in gestational diabetes: heterogeneity in the number and a novel abnormality in subcellular localization of GLUT4 glucose transporters. Diabetes. 42:1773-1785.
17. Pederson, O., J.F. Bak, P.H. Andersen, S. Lund, D.E. Moller, J.S. Flier, and B.B. Kahn. 1990. Evidence against altered expression of GLUT1 or GLUT4 in skeletal muscle of patients with obesity or NIDDM. Diabetes. 39: 865-870.
18. Garvey, W.T., L. Maianu, J.A. Hancock, A.M. Golichowski, and A. Baron. 1992. Gene expression of GLUT4 in skeletal muscle from insulin-resistant patients with obesity, IGT, GDM, and NIDDM. Diabetes. 41:405-175.
19. Zierath, J.R., L. He, A. Guma, E.O. Wahlstrom, A. Klip, and H. Walberg-Henriksson. 1996. Insulin action on glucose transport and plasma membrane GLUT4 content in skeletal muscle from patients with NIDDM. Diabetologia. 39:1180-1189.
20. Goodyear, L.J., F. Giorgino, L.A. Sherman, J. Carey, R.J. Smith, and G.L. Dohm. 1995. Insulin receptor phosphorylation, insulin receptor substrate-1 phosphorylation, and phosphatidylinositol 3-kinase activity are decreased in intact skeletal muscle strips from obese subjects. J. Clin. Invest. 95:2195-2204.
21. Czeck, M.P. 1995. Molecular actions of insulin on glucose transport. Annu. Rev. Nutr. 15:441-471.
22. Cheatham, B., A. Volchuk, C.R. Kahn, L. Wang, C.J. Rhodes, and A. Klip. 1996. Insulin-stimulated translocation of GLUT4 glucose transporters requires SNARE-complex proteins. Proc. Natl. Acas. Sci. USA. 93:15169-15173.
23. Timmers, K.I., A.E. Clark, M. Omatsu-Kanbe, S.W. Whiteheart, M.K. Bennett, G.D. Holman, and S.W. Cushman. 1996. Identification of SNAP receptors in rat adipose cell membrane fractions and in SNARE complexes co-immunoprecipitated with epitope-lagged N-ethylmaleimide-sensitive fusion protein. Biochem. J. 320:429-436.
24. Sollner, T.H., and J.E. Rothman. 1996. Molecular machinery mediating vesicle budding, docking, and fusion. Cell Struct. Funct. 21:407-412.
25. Sudhof, T.C. 1995. The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature. 375:645-653.
26. National Diabetes Data Group. 1979. Classification and diagnosis of diabetes mellitus and other categories of glucose intolerance. Diabetes. 28:1039-1057.
27. Garvey, W.T., J.M. Olefsky, J. Griffin, R.F. Hamman, and O.G. Kolterman. 1985. The effect of insulin treatment on insulin secretion and insulin action in type II diabetes mellitus. Diabetes. 34:222-234.
28. Baron, A., M. Laakso, G. Brechtel, and S.V. Edelman. 1991. Reduced capacity and affinity of skeletal muscle for insulin-mediated glucose uptake in non-insulin-dependent diabetic subjects. J. Clin. Invest. 87:1186-1194.
29. Klip, A., T. Ramlal, D.A. Young, and J.O. Holloszy. 1987. Insulin-induced translocation of glucose transporter in rat hindlimb muscles. FEBS (Fed. Eur. Biochem. Soc.) Lett. 224:224-230.
30. Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:680-685.
31. Towbin, H., T. Staehelin, and J. Gordon. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA. 76:4350-4354.
32. Jorgensen, A.O., and L.R. Jones. 1986. Localization of phospholamban in slow but not fast canine skeletal muscle fibers: an immunocytochemical and biochemical study. J. Biol. Chem. 261:3775-3781.
33. Palmer, C.J., B.T. Scott, and L.R. Jones. 1991. Purification and complete sequence determination of the major plasma membrane substrate for c-AMP-dependent protein kinase and protein kinase C in myocardium. J. Biol. Chem. 266:11126-11130.
34. Moorman, J.R., C.J. Palmer, J.E. John, M.E. Durieux, and L.R. Jones. 1992. Phospholemman expression induces a hyperpolarization-activated chloride current in Xenopus oocytes. J. Biol. Chem. 267:14551-14554.
35. Morton, M.E., J.M. Caffrey, A.M. Brown, and S.C. Froehner. 1988. Monoclonal antibody to the alpha 1-subunit of the dihydropyridine-binding complex inhibits calcium currents in BC3H1 myocytes. J. Biol. Chem. 263:613-616.
36. Keller, S.R., H.M. Scott, C.C. Mastick, R. Aebersold, and G.E. Lienhard. 1995. Cloning and characterization of a novel insulin-regulated membrane aminopeptidase from GLUT4 vesicles. J. Biol. Chem. 270:23612-23618.
37. Kandror, K.V., and P.F. Pilch. 1994. gp160, a tissue specific marker for insulin-activated glucose transport. Proc. Acad. Sci. USA. 91:8017-8021.
38. Bradford, M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle protein-dye bonding. Anal. Biochem. 72:248-254.
39. Martin, S., J.E. Rice, G.W. Gould, S.R. Keller, J.W. Slot, and D.E. James. 1947. The glucose transporter GLUT4 and the aminopeptidase vp165 colocalise in tubulo-vesicular elements in adipocytes and cardiomyocytes. J. Cell. Sci. 110:2281-2291.
40. Filippis, A., S. Clark, and J. Proietto. 1998. Possible role for gp160 in constitutive hut not insulin-stimulated GLUT4 trafficking: dissociation of gp160 and GLUT4 localization. Biochem. J. 330:405-411.
41. Aledo, J.C., L. Lavoie, A. Volchuk, S.R. Keller, A. Klip, and H.S. Hundal. 1997. Identification and characterization of two distinct intracellular GLUT4 pools in rat skeletal muscle: evidence for an endosomal and an insulin-sensitive GLUT4 compartment. Biochem. J. 325 (Pt. 3):727-732.
42. Baron, A.D., J.-S. Zhu, J.-H. Zhu, H. Weldon, L. Maianu, and W.T. Garvey. 1995. Glucosamine induces insulin resistance in vivo by affecting GLUT4 translocation in skeletal muscle: implications for glucose toxicity. J. Clin. Invest. 96:2792-2801.
43. Sternlicht, E., R.J. Barnard, and G.K. Grimditch. 1988. Mechanism of insulin action on glucose transport in rat skeletal muscle. Am. J. Physiol. 254: E633-E638.
44. Hirshman, M.F., L.J. Goodyear, L.J. Wardzala, E.D. Horton, and E.S. Horton. 1990. Identification of an intracellular pool of glucose transporters from basal and insulin-stimulated rat skeletal muscle. J. Biol. Chem. 265:987-991.
45. Lund, S., H. Vestergaard, P.H. Andersen, O. Schmitz, L.B. Gotzsche, and O. Pedersen. 1993. GLUT4 content in plasma membrane of muscle from patients with non-insulin-dcpendent diabetes mellitus. Am. J. Physiol. 265: E889-E897.
46. Guma, A., J.R. Zierath, H. Wallberg-Henriksson, and A. Klip. 1995. Insulin induces translocation of GLUT4 glucose transporters in human skeletal muscle. Am. J. Physiol. 268:E613-E622.
47. Friedman, J.E., R.W. Dudek, D.S. Whitehead, D.L. Downes, W.R. Frisell, J.F. Caro, and G.L. Dohm. 1991. Immunolocalization of glucose transporter GLUT4 within human skeletal muscle. Diabetes. 40:150-154.
48. Munoz, P., M. Rosemblatt, X. Testar, M. Palacin, G. Thoidis, P.F. Pilch, and A. Zorzano. 1995. The T-tubule is a cell-surface target for insulin-regulated recycling of membrane proteins in skeletal muscle. Biochem. J. 312 (Pt. 2):393-400.
49. Dombrowski, L., D. Roy, B. Marcotte, and A. Marette. 1996. A new procedure for the isolation of plasma membranes. T-tubules, and internal membranes from skeletal muscle. Am. J. Physiol. 270:E667-E676.
50. Wang, W., P.A. Hansen, B.A. Marshall, J.O. Holloszy, and M. Mueckler. 1996. Insulin unmasks a COOH-terminal GLUT4 epitope and increases glucose transport across t-tubules in skeletal mucle. J. Cell Biol. 135:415-430.
51. Hollenbeck, C. and G.M. Reaven. 1987. Variations in insulin-stimulated glucose uptake in healthy individuals with normal glucose tolerance. J. Clin. Endocrinol. Metab. 64:1169-1173.
52. Bogardus, C., and S. Lillioja. 1992. Pima Indians as a model to study the genetics of NIDDM. J. Cell. Biochem. 48:337-343.
53. Garvey, W.T., L. Maianu, G. Brechtel, A. Johnson, K. Sunblad, and D. Hardin. 1994. Muscle GLUT4 expression is a familial trait and determines insulin sensitivity in humans independent of obesity. Diabetes. 43 (Suppl. 1):69a.
54. Maianu, L., S. Keller, and W.T. Garvey. 1996. Fat and muscle express a common abnormality in translocation/trafficking of GLUT4/vp165 containing vesicles in NIDDM. Diabetes. 45 (Suppl. 2):157a.
55. Garvey, W.T., J.M. Olefsky, S. Matthaei, and S. Marshall. 1987. Glucose and insulin coregulate the glucose transport system in primary cultured adipocytes: a new mechanism of insulin resistance. J. Biol. Chem. 262:189-197.
56. Kin, P.A., E.D. Horton, M.F. Hirshman, and E.S. Horton. 1992. Insulin resistance in obese Zucker rat (fa/fa) skeletal muscle is associated with a failure of glucose transporter translocation. J. Clin. Invest. 90:1568-1575.