Insulin unmasks a COOH-terminal Glut4 epitope and increases glucose transport across T-tubules in skeletal muscle

Journal of Cell Biology

Volumn 135, Issue 2, 1996, Pages 415-430

  Wang, Weichen ^a   Hansen, Polly A ^a   Marshall, Bess A ^a   Holloszy, John O ^a   Mueckler, Mike ^a,b  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Dept of Cell Biology and Physiology ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; GLUCOSE; GLUCOSE TRANSPORTER; INSULIN;

ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; GLUCOSE TRANSPORT; IMMUNOGOLD STAINING; MOUSE; NONHUMAN; PRIORITY JOURNAL; RAT; SARCOLEMMA; SKELETAL MUSCLE; TRANSGENIC MOUSE; TRANSVERSE TUBULAR SYSTEM;

ANIMALS; EPITOPES; GLUCOSE; GLUCOSE TRANSPORTER TYPE 1; GLUCOSE TRANSPORTER TYPE 4; HISTOLOGICAL TECHNIQUES; HUMANS; INFUSIONS, INTRAVENOUS; INJECTIONS, INTRAPERITONEAL; INSULIN; MICE; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; MICROSCOPY, IMMUNOELECTRON; MICROTUBULES; MONOSACCHARIDE TRANSPORT PROTEINS; MUSCLE PROTEINS; MUSCLE, SKELETAL; RATS; RECOMBINANT PROTEINS; SARCOLEMMA; SUBCELLULAR FRACTIONS; TISSUE EMBEDDING;

ANIMALIA; MUS MUSCULUS;

EID: 0029862135     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.135.2.415     Document Type: Article

References (55)

1. Baron, A.D., H. Steinberg, G. Brechtel, and A. Johnson. 1994. Skeletal muscle blood flow independently modulates insulin-mediated glucose uptake. Am. J. Physiol. 266:E248-E253.
2. Birks, R.I., and D.F. Davey. 1969. Osmotic responses demonstrating the extracellular character of the sarcoplasmic reticulum. J. Physiol. 202: 171-188.
3. Birnbaum, M.J. 1989. Identification of a novel gene encoding an insulin-responsive glucose transporter protein. Cell. 57:305-315.
4. Birnbaum, M.J., H.C. Haspel, and O.M. Rosen. 1986. Cloning and characterization of a cDNA encoding the rat brain glucose-transporter protein. Proc. Natl. Acad. Sci. USA. 83:5784-5788.
5. Bonadonna, R.C., P.S. Del, M.P. Saccomani, E. Bonora, O. 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. Bornemann, A., T. Ploug, and H. Schmalbruch. 1992. Subcellular localization of GLUT4 in nonstimulated and insulin-stimulated soleus muscle of rat. Diabetes. 41:215-221.
7. Charron, M.J., F.D. Brosius, S.L. Alper, and H.F. Lodish. 1989. A glucose transport protein expressed predominately in insulin-responsive tissues. Proc. Natl. Acad. Sci. USA. 86:2535-2539.
8. Corvera, S., A. Chawla, R. Chakrabarti, M. Joly, J. Buxton, and M.P. Czech. 1994. A double leucine within the GLUT4 glucose transporter COOH-terminal domain functions as an endocytosis signal. (Published erratum appears in J. Cell Biol. 1994, 126:1625.) J. Cell Biol. 126:979-989.
9. Cushman, S.W., and L.J. Wardzala. 1980. Potential mechanism of insulin action on glucose transport in the isolated rat adipose cell. Apparent translocation of intracellular transport systems to the plasma membrane. J. Biol. Chem. 255:4758-4762.
10. Dohm, G.L., P.L. Dolan, W.R. Frisell, and R.W. Dudek. 1993. Role of transverse tubules in insulin stimulated muscle glucose transport. J. Cell Biochem. 52:1-7.
11. Douen, A.G., E. Burdett, T. Ramlal, S. Rastogi, M. Vranic, and A. Klip. 1991. Characterization of glucose transporter-enriched membranes from rat skeletal muscle: assessment of endothelial cell contamination and presence of sarcoplasmic reticulum and transverse tubules. Endocrinology. 128:611-616.
12. 3H]BMPA photolabel. FEBS Lett. 339: 205-208.
13. Eisenberg, B., and R.S. Eisenberg. 1968. Selective disruption of the sarcotubular system in frog sartorius muscle. J. Cell Biol. 39:451-467.
14. Eisenberg, B.R., and R.S. Eisenberg. 1982. The T-SR junction in contracting single skeletal muscle fibers. J. Gen. Physiol. 79:1-19.
15. Eisenberg, R.S., J.N. Howell, and P.C. Vaughan. 1971. The maintenance of resting potentials in glycerol-treated muscle fibres. J. Physiol. 215:95-102.
16. El-Kebbi, I.M., S. Roser, R.J. Pollet, S.W. Cushman, and C.M. Wilson. 1994. Regulation of the GLUT1 glucose transporter in cultured myocytes: total number and subcellular distribution as determined by photoaffinity labeling. Biochem. J. 301:35-40.
17. Ferrannini, E., O. Bjorkman, G.A. Reichard, A. Pilo, M. Olsson, J. Wahren, and R.A. DeFronzo. 1985. The disposal of an oral glucose load in healthy subjects. Diabetes. 34:580-588.
18. 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.
19. Fukumoto, H., T. Kayano, J.B. Buse, V. Edwards, P.F. Pilch, G.I. Bell, and S. Seino. 1989. Cloning and characterization of the major insulin-responsive glucose transporter expressed in human skeletal muscle and other insulin-responsive tissues. J. Biol. Chem. 264:7776-7779.
20. Gate, P.W., and R.S. Eisenberg. 1967. Action potentials without contraction in frog skeletal muscle fibers with disrupted transverse tubules. Science (Wash. DC). 158:1702-1703.
21. Gulve, E.A., J.M. Ren, B.A. Marshall, J. Gao, P.A. Hansen, J.O. Holloszy, and M. Mueckler. 1994. Glucose transport activity in skeletal muscles from transgenic mice overexpressing GLUT1. Increased basal transport is associated with a defective response to diverse stimuli that activate GLUT4. J. Biol. Chem. 269:18366-18370.
22. Haney, P.M., J.W. Slot, R.C. Piper, D.E. James, and M. Mueckler. 1991. Intracellular targeting of the insulin-regulatable glucose transporter (GLUT4) is isoform specific and independent of cell type. J. Cell Biol. 114:689-699.
23. Haney, P.M., M.A. Levy, M.S. Strube, and M. Mueckler. 1995. Insulin-sensitive targeting of the GLUT4 glucose transporter in L6 myoblasts is conferred by its COOH-terminal cytoplasmic tail. J. Cell Biol. 129:641-658.
24. Hansen, P.A., E.A. Gulve, B.A. Marshall, J. Gao, J.E. Pessin, J.O. Holloszy, and M. Mueckler. 1995. Skeletal muscle glucose transport and metabolism are enhanced in transgenic mice overexpressing the Glut4 glucose transporter. J. Biol. Chem. 270:1679-1684.
25. 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.
26. Holman, G.D., I.J. Kozka, A.E. Clark, C.J. Flower, J. Saltis, A.D. Habberfield, I.A. Simpson, and S.W. Cushman. 1990. Cell surface labeling of glucose transporter isoform GLUT4 by bis-mannose photolabel. Correlation with stimulation of glucose transport in rat adipose cells by insulin and phorbol ester. J. Biol. Chem. 265:18172-18179.
27. Hresko, R.C., M. Kruse, M. Strube, and M. Mueckler. 1994. Topology of the Glut 1 glucose transporter deduced from glycosylation scanning mutagenesis. J. Biol. Chem. 269:20482-20488.
28. Hresko, R.C., H. Murata, B.A. Marshall, and M. Mueckler. 1994. Discrete structural domains determine differential endoplasmic reticulum to Golgi transit times for glucose transporter isoforms. J. Biol. Chem. 269: 32110-32119.
29. James, D.E., M. Strube, and M. Mueckler. 1989. Molecular cloning and characterization of an insulin regulatable glucose transporter. Nature (Lond.). 338:83-87.
30. Krolenko, S.A. 1969. Changes in the T-system of muscle fibres under the influence of influx and efflux of glycerol. Nature (Lond.). 221:966-968.
31. Liu, M.-L., E.M. Gibbs, S.C. McCoid, A.J. Milici, H.A. Stukenbrok, R.K. McPherson, J.L. Treadway, and J.E. Pessin. 1993. Transgenic mice expressing the human GLUT4/muscle-fat facilitative glucose transporter protein exhibit efficient glycemic control. Proc. Natl. Acad. Sci. USA. 90: 11346-11350.
32. Marette, A., E. Burdett, A. Douen, M. Vranic, and A. Klip. 1992. Insulin induces the translocation of GLUT4 from a unique intracellular organelle to transverse tubules in rat skeletal muscle. Diabetes. 41:1562-1569.
33. Marette, A., J.M. Richardson, T. Ramlal, T.W. Balon, M. Vranic, J.E. Pessin, and A. Klip. 1992. Abundance, localization, and insulin-induced translocation of glucose transporters in red and white muscle. Am. J. Physiol. 263:C443-C452.
34. Marshall, B.A., and M.M. Mueckler. 1994. Differential effects of GLUT-1 or GLUT-4 overexpression on insulin responsiveness in transgenic mice. Am. J. Physiol. 267:E738-E744.
35. Marshall, B.A., H. Murata, R.C. Hresko, and M. Mueckler. 1993. Domains that confer intracellular sequestration of the Glut4 glucose transporter in Xenopus oocytes. J. Biol. Chem. 268:26193-26199.
36. Marshall, B.A., J.M. Ren, D.W. Johnson, E.M. Gibbs, J.S. Lillquist, W.C. Soeller, J.O. Holloszy, and M. Mueckler. 1993. Germline manipulation of glucose homeostasis via alteration of glucose transporter levels in skeletal muscle. J. Biol. Chem. 268:18442-18445.
37. Mitchell, R.D., P. Palade, and S. Fleischer. 1983. Purification of morphologically intact triad structures from skeletal muscle. J. Cell Biol. 96:1008-1016.
38. Mueckler, M. 1995. Glucose transport and glucose homeostasis: new insights from transgenic mice. News Physiol. Sci. 10:22-29.
39. Mueckler, M., C. Caruso, S.A. Baldwin, M. Panico, I. Blench, H.R. Morris, W.J. Allard, G.E. Lienhard, and H.F. Lodish. 1985. Sequence and structure of a human glucose transporter. Science (Wash. DC). 229:941-945.
40. Munoz, P., M. Rosemblatt, X. Testar, M. Palacin, G. Thoidis, P.F. Pilch, and A. Zorzano. 1996. The T-tubule is a cell-surface target for insulin-regulated recycling of membrane proteins in skeletal muscle. Biochem. J. 312:393-400.
41. Nakajima, S., Y. Nakajima, and L.D. Peachey. 1973. Speed of repolarization and morphology of glycerol-treated frog muscle fibres. J. Physiol. 234:465-480.
42. Olson, A.L., M.L. Liu, R.W.S. Moye, J.B. Buse, G.I. Bell, and J.E. Pessin. 1993. Hormonal/metabolic regulation of the human GLUT4/muscle-fat facilitative glucose transporter gene in transgenic mice. J. Biol. Chem. 268:9839-9846.
43. Parekh, B.S., P.W. Schwimmbeck, and M.J. Buchmeier. 1989. High efficiency immuno-affinity purification of anti-peptide antibodies on thiopropyl Sepharose immunoadsorbants. Pept. Res. 2:249-252.
44. Ren, J.M., B.A. Marshall, E.A. Gulve, J. Gao, D.W. Johnson, J.O. Holloszy, and M. Mueckler. 1993. Evidence from transgenic mice that glucose transport is rate-limiting for glycogen deposition and glycolysis in skeletal muscle. J. Biol. Chem. 268:16113-16115.
45. Rodnick, K.J., J.W. Slot, D.R. Studelska, D.E. Hanpeter, L.J. Robinson, H.J. Geuze, and D.E. James. 1992. Immunocytochemical and biochemical studies of GLUT4 in rat skeletal muscle. J. Biol. Chem. 267:6278-6285.
46. 31P nuclear magnetic resonance measurements of muscle glucose-6-phosphate. Evidence for reduced insulin-dependent muscle glucose transport or phosphorylation activity in non-insulin-dependent diabetes mellitus. J. Clin. Invest. 89:1069-1075.
47. Rubio, R., and N. Sperelakis. 1972. Penetration of horseradish peroxidase into the terminal cisternae of frog skeletal muscle. Z. F. Zellforsc. Mikrosk. Anat. 124:57-71.
48. Slot, J.W., H.J. Geuze, S. Gigengack, G.E. Lienhard, and D.E. James. 1991. Immune-localization of the insulin regulatable glucose transporter in brown adipose tissue of the rat. J. Cell Biol. 113:123-135.
49. Smith, R.M., M.J. Charron, N. Shah, H.F. Lodish, and L. Jarett. 1991. Immunoelectron microscopic demonstration of insulin-stimulated translocation of glucose transporters to the plasma membrane of isolated rat adipocytes and masking of the carboxyl-terminal epitope of intracellular GLUT4. Proc. Natl. Acad. Sci. USA. 88:6893-6897.
50. Treadway, J.L., D.M. Hargrove, N.A. Nardone, R.K. McPherson, J.F. Russo, A.J. Milici, H.A. Stukenbrok, E.M. Gibbs, R.W. Stevenson, and J.E. Pessin. 1994. Enhanced peripheral glucose utilization in transgenic mice expressing the human GLUT4 gene. J. Biol. Chem. 269:29956-29961.
51. Verhey, K.J., and M.J. Birnbaum. 1994. A Leu-Leu sequence is essential for COOH-terminal targeting signal of GLUT4 glucose transporter in fibroblasts. J. Biol. Chem. 269:2353-2356.
52. Verhey, K.J., J.I. Yeh, and M.J. Birnbaum. 1995. Distinct signals in the GLUT4 glucose transporter for internalization and for targeting to an insulin-responsive compartment. J. Cell Biol. 130:1071-1079.
53. Wilson, C.M., and S.W. Cushman. 1994. Insulin stimulation of glucose transport activity in rat skeletal muscle: increase in cell surface GLUT4 as assessed by photolabeling. Biochem. J. 299:755-759.
54. Young, D.A., H.J. Uhl, G.D. Cartee, and J.O. Holloszy. 1986. Activation of glucose transport in muscle by prolonged exposure to insulin. J. Biol. Chem. 261:16049-16053.
55. Zorzano, A., W. Wilkinson, N. Kotliar, G. Thoidis, B.E. Wadzinkski, A.E. Ruoho, and P.F. Pilch. 1989. Insulin-regulated glucose uptake in rat adipocytes is mediated by two transporter isoforms present in at least two vesicle populations. J. Biol. Chem. 264:12358-12363.