GLUT4: a key player regulating glucose homeostasis? Insights from transgenic and knockout mice

References

• Abel, E. D., Peroni, O., Kim, J. K., Kim, Y. B., Boss, O., Hadro, E ., Minnemann, T., Shulman, G. I. and Kahn, B. B., 2001, Adipose- s electiv e targeting of the GLUT4 gene impairs insulin action in muscle and liver. Nature, 409, 729 ± 733.
   PubMed Web of Science ®Google Scholar
• AndreÂasson, K., Galuska, D., ThoÈrne, A., Sonnenfeld, T. and Wallberg-Henriksson, H., 1991, Decreas ed insulin-stimulated 3- O-methylglucos e transport in in vitro incubated muscle strips from type II diabetic subjects. Acta Physiologica Scandinavica, 142, 255 ± 260.
   Google Scholar
• Bao, S. and Garvey, W. T., 1997, Exercis e in transgenic mice overexpressing GLUT4 glucos e transporters: effects on substrate metabolis m and glycogen regulation. Metabolism, 46, 1349 ± 1357.
   Google Scholar
• Birnbaum, M. J., 1989, Identifica tion of a novel gene encoding an insulin-responsive glucose transporter protein. Cell, 57, 305 ± 315. Birnbaum, M. J., Haspel, H. C. and Ros en, O. M., 1986, Cloning and characterization of a cDNA encoding the rat brain glucos e- transporter protein. Proceedings of the National Academy of Sciences (USA), 83, 5784 ± 5788.
   Google Scholar
• Brozinick Jr., J. T., McCoid, S. C., Reynolds, T. H., Nardone, N. A., Hargrove, D. M., Stevenson, R. W., Cushman, S. W. and Gibbs, E. M., 2001, GLUT4 overexpression in db/db mice dose- dependently ameliorates diabetes but is not a lifelong cure. Diabetes, 50, 593 ± 600.
   Google Scholar
• Brozinick Jr., J. T., McCoid, S. C., Reynolds, T. H., Wilson, C. M., Stevenson, R. W., Cushman, S. W. and Gibbs, E. M., 1997, Regulation of cell surface GLUT4 in skeleta l muscle of transgenic mice. Biochemistry Journal, 321, 75 ± 81.
   Google Scholar
• Brozinick Jr., J. T., Yaspelkis 3rd, B. B., Wilson, C. M., Grant, K. E ., Gibbs, E. M., Cushman, S. W. and Ivy, J. L., 1996, Glucose transport and GLUT4 protein distribution in skeletal muscle of GLUT4 transgenic mice. Biochemistry Journal, 313, 133 ± 140. Cartee, G. D., Douen, A. G., Ramlal, T., Klip, A. and Holloszy, J. O., 1991, Stimulation of glucos e transport in skeleta l muscle by hypoxia. Journal of Applied Physiology, 70, 1593 ± 1600.
   Google Scholar
• Charron, M. J., Brosius, F. C., Alper, S. L. and Lodish, H. L., 1989, A glucos e transport protein express ed predominately in insulin- s ensitive tissues. Proceedings of the National Academy of Sciences (USA), 86, 2535 ± 2539.
   PubMedGoogle Scholar
• Chibalin, A. V., Yu, M., Ryder, J. W., Song, X. M., Galuska, D., Krook, A., Wallberg-Henriksson, H. and Zierath, J. R., 2000, Exercis e-induced changes in expression and activity of proteins involved in insulin signal transduction in skeletal muscle: differentia l effects on insulin receptor substrates 1 and 2. Proceedings of the National Academy of Sciences (USA), 97, 38 ± 43.
   PubMed Web of Science ®Google Scholar
• Deems, R. O., Evans, J. L., Deacon, R. W., Honer, C. M., Chu, D. T.,Burki, K., Fillers, W. S., Cohen, D. K. and Young, D. A., 1994, Expression of human GLUT4 in mice results in increas ed insulin action. Diabetologia, 37, 1097 ± 1104.
   Google Scholar
• DeFronzo, R. A., 1988, The triumvirate: b-cell, muscle or liver. A collusion responsible for NIDDM. Diabetes, 37, 667 ± 687.
   PubMed Web of Science ®Google Scholar
• DeFronzo, R. A., Gunnarsson, R., BjoÈrkman, O., Olsson, M. and Wahren, J., 1985, Effects of insulin on peripheral and splanchnic glucos e metabolis m in non-insulin-dependent (Type II) diabetes mellitus. Journal of Clinica l Investigations, 76, 149 ± 155.
   PubMed Web of Science ®Google Scholar
• Doege, H., Bocianski, A., Joost, H. G. and SchuÈrmann, A., 2000b, Activity and genomic organization of human glucose transporter 9 (GLUT9), a novel member of the family of sugar-transport facilitator s predominantly express ed in brain and leucocytes. Biochemistry Journal, 350, 771 ± 776.
   PubMedGoogle Scholar
• Doege, H., SchuÈrmann, A., Bahrenberg, G., Brauers, A. and Joost, H.-G., 2000a, GLUT8, A novel member of the sugar transport facilitator family with glucos e transport activity. Journal of Biologica l Chemistry, 275, 16275 ± 16280.
   PubMed Web of Science ®Google Scholar
• Douen, A. G., Ramlal, T., Rastogi, S. A., Bilan, P. J., Cartee, G. D., Vranic, M., Holloszy, J. O. and Klip, A., 1990, Exercis e induces recruitment of the `insulin responsive’ glucos e transporter. Evidence for distinct intracellula r insulin- and exercise-recruitabl e transporter pools in skeleta l muscle. Journal of Biological Chemistry, 265, 13427 ± 13430.
   PubMedGoogle Scholar
• Gibbs, E. M., Stock, J. L., McCoid, S. C., Stukenbrok, H. A., Pessin,J. E., Stevenson, R. W., Milici, A. J. and Ncneish, J. D., 1995, Glycemic improvement in diabetic db/db mice by overexpression of the human insulin-regulatable glucos e transporter (GLUT4). Journal of Clinica l Investigations, 95, 1512 ± 1518.
   PubMed Web of Science ®Google Scholar
• Handberg, A., Kays er, L., Hoyer, P. E. and Vinten, J., 1992, A substantia l part of GLUT-1 in crude membranes from muscle originates from perineurial sheaths. American Journal of Physiol- ogy and Endocrinology Metabolis m (Endocrinology Metabolism), 262, E 721 ± E727.
   Google Scholar
• Hansen, P. A., Gulve, E. A., Marshall, B. A., Gao, J., Pessin, J. E., Holloszy, J. O. and Mueckler, M. M., 1995, Skeleta l muscle glucos e transport and metabolis m are enhanced in transgenic mice overexpress ing the GLUT4 glucos e transporter. Journal of Biologica l Chemistry, 270, 1679 ± 1684.
   PubMedGoogle Scholar
• Hjeltnes, N., Galuska, D., BjoÈrnholm, M., Aksnes, A.-K., Lannem, A., Zierath, J. R. and Wallberg-Henriksson, H., 1998, E xercis e- induced overexpression of key regulatory proteins involved in glucos e uptake and metabolis m in tetraplegic persons: molecular mechanism for improved glucos e homeostasis. FASEB Journal, 12, 1701 ± 1712.
   PubMed Web of Science ®Google Scholar
• Hughes, V. A., Fiatarone, M. A., Fielding, R. A., Kahn, B. B., Ferrara,M., Shepherd, P. R., Fisher, E. C., Wolfe, R. R., Elahi, D. and Evans, W. J., 1993, Exercis e increas es muscle GLUT4-levels and insulin action in subjects with impaired glucose tolerance. American Journal of Physiology (Endocrinology Metabolism), 264, E 855 ± E862.
   Google Scholar
• Hundal, H. S., Ahmed, A., Guma, A., Mitsumoto, Y., Marette, A., Rennie, M. J. and Klip, A., 1992, Biochemical and immunocyto- chemical localization of the GLUT5 glucos e transporter in human skeletal muscle. Biochemistry Journal, 286, 339 ± 343.
   Google Scholar
• Ibberson, M., Uldry, M. and Thorens, B., 2000, GLUTX1, a novel mammalian glucos e transporter express ed in the central nervous system and insulin-s ensitive tissues. Journal of Biological Chem- istry, 275, 4607 ± 4612.
   PubMed Web of Science ®Google Scholar
• Ikemoto, S., Thompson, K. S., Takahashi, M., Itakura, H., Lane, M.and Ezaki, O., 1995, High fat diet-induced hyperglycemia: prevention by low level expression of a glucos e transporter (GLUT4) minigene in transgenic mice. Proceedings of the National Academy of Sciences (USA), 92, 3096 ± 3099.
   PubMed Web of Science ®Google Scholar
• Ishizuka, T., Klepcyk, P., Liu, S., Panko, L., Liu, S., Gibbs, E. M. and Friedman, J. E., 1999, Effects of overexpression of human GLUT4 gene on maternal diabetes and feta l growth in spontaneous gestational diabetic C57BLKS/J Lepr(db/+) mice. Diabetes, 48, 1061 ± 1069.
   Google Scholar
• James, D. E., Strube, M. M. and Mueckler, M. M., 1989, Molecular cloning and characterizatio n of an insulin-regulatable glucos e transporter. Nature, 338, 83 ± 87.
   PubMedGoogle Scholar
• Kahn, B. B., Ross etti, L., Lodish, H. F. and Charron, M. J., 1991, Decreas ed in vivo glucos e uptake but normal expression of GLUT1 and GLUT4 in skeleta l muscle of diabetic rats. Journal of Clinical Investigations, 87, 2197 ± 2206.
   Google Scholar
• Katz, E. B., Stenbit, A. E., Hatton, K., DePinho, R. and Charron, M. J., 1995, Cardiac and adipos e tissue abnormalities but not diabetes in mice deficient in GLUT4. Nature, 377, 151 ± 155.
   PubMed Web of Science ®Google Scholar
• Koranyi, L., James, D., Mueckler, M. and Permutt, M. A., 1990,Glucos e transporter levels in spontaneously obes e (db/db) insulin- resistant mice. Journal of Clinical Investigations, 85, 962 ± 967.
   Google Scholar
• Krook, A., BjoÈrnholm, M., Galuska, D., Jiang, X.-J., Fahlman, R., Myers Jr., M. G., Wallberg-Henriksson, H. and Zierath, J. R., 2000, Characterization of signal transduction and glucose trans- port in skeletal muscle from type 2 diabetic patients. Diabetes, 49, 284 ± 292.
   Google Scholar
• Lee, A. D., Hansen, P. A. and Holloszy, J. O., 1995, Wortmannin inhibits insulin-stimulated but not contraction-stimulated glucos e transport activity in skeletal muscle. FEBS Letters, 361, 51 ± 54.
   PubMed Web of Science ®Google Scholar
• Leturque, A., Loiz eau, M., Vaulont, S., Salminen, M. and Girard, J., 1996, Improvement of insulin action in diabetic transgenic mice s electively overexpress ing GLUT4 in skeletal muscle. Diabetes, 45, 23 ± 27.
   Google Scholar
• Liu, M.-L., Gibbs, E. M., McCoid, S. C., Milici, A. J., Stukenbrok, H. A., McPherson, R. K., Treadway, J. L. and Pessin, J. E., 1993, Transgenic mice expressing the human GLUT4/muscle-fat facil- itativ e glucos e transporter protein exhibit efficient glycemic control. Proceedings of the National Academy of Sciences (USA), 90, 11346 ± 11350.
   PubMed Web of Science ®Google Scholar
• Lund, S., Holman, G. D., Schmitz, O. and Peders en, O., 1995, Contraction stimulates translocation of glucos e transporter GLUT4 in skeletal muscle through a mechanism distinct from that of insulin. Proceedings of the National Academy of Sciences (USA), 92, 5817 ± 5821.
   Google Scholar
• Marette, A., Burdett, E., Douen, A., Vranic, M. and Klip, A., 1992, Insulin induces the translocation of GLUT4 from a unique intracellula r organelle to transvers e tubules in rat skeletal muscle. Diabetes, 12, 1562 ± 1569.
   Google Scholar
• Marshall, B. A. and Mueckler, M. M., 1994, Differentia l effects of GLUT1 or GLUT4 overexpression on insulin responsiveness in transgenic mice. American Journal of Physiology (Endocrinology Metabolism), 267, E738 ± E 744.
   Google Scholar
• Mueckler, M., Caruso, C., Baldwin, S. A., Panico, M., Blench, I.,Morris, H. R., Allard, W. J., Lienhard, G. E. and Lodish, H. F., 1985, Sequence and structure of a human glucose transporter. Science, 229, 941 ± 945.
   PubMed Web of Science ®Google Scholar
• Ren, J.-M., Marshall, B. A., Mueckler, M. M., McCaleb, M., Amatruda, J. M. and Schulman, G. I., 1995, Overexpression of GLUT4 protein in muscle increas es basal and insulin-stimulated whole body glucose disposal in conscious mice. Journal of Clinica l Investigations, 95, 429 ± 432.
   PubMedGoogle Scholar
• Ren, J.-M., Semenkovich, C. F., Gulve, E. A., Gao, J. and Holloszy,J. O., 1994, Exercis e induces rapid increases in GLUT4 expression, glucos e transport capacity, and insulin-stimulated glycogen storage in muscle. Journal of Biologica l Chemistry, 269, 14396 ± 14401.
   PubMed Web of Science ®Google Scholar
• Rodgers, M. A., Yamamoto, C., King, D. S., Hagberg, J. M., Ehsani,A. A. and Holloszy, J. O., 1988, Improvement in glucose tolerance after 1 wk of exercis e in patients with mild NIDDM. Diabetes Care, 11, 613 ± 618.
   PubMedGoogle Scholar
• Rossetti, L., Stenbit, A. E., Chen, W., Hu, M., Barzilai, N., Katz, E. B. and Charron, M. J., 1997, Peripheral but not hepatic insulin resistance in mice with one disrupted allele of the glucos e transporter type 4 (GLUT4) gene. Journal of Clinical Investiga- tions, 100, 1831 ± 1839.
   Google Scholar
• Ryder, J. W., Kawano, Y., Chibalin, A. V., Rincon, J., Tsao, T.-S., Stenbit, A. E ., Combatsiaris, T., Yang, J., Holman, G. D. and Zierath, J. R., 1999a, In vitro analysis of the glucos e-transport system in GLUT4-null skeletal muscle. Biochemistry Journal, 342, 321 ± 328. Ryder, J. W., Kawano, Y., Galuska, D., Fahlman, R., Wallberg- Henriksson, H., Charron, M. J. and Zierath, J. R., 1999b, Post- exercis e glucos e uptake and glycogen synthesis in skeletal muscle from GLUT4-deficient mice. FASEB Journal, 13, 2246 ± 2256. Shepherd, P. R., Gibbs, E. M., Wesslau, C., Gould, G. W. and Kahn, B. B., 1992, Human small intestine facilitativ e fructos e/glucos e transporter (GLUT5) is also present in insulin-responsive tissues and brain. Investigation of biochemical characteristic s and translocation. Diabetes, 10, 1360 ± 1365.
   Google Scholar
• Shepherd, P. R., Gnudi, L., Tozzo, E., Yang, H., Leach, F. and Kahn,B. B., 1993, Adipos e cell hyperplasia and enhanced glucos e disposal in transgenic mice overexpressing GLUT4 s electively in adipose tissue. Journal of Biological Chemistry, 268, 22243 ± 22246.
   PubMed Web of Science ®Google Scholar
• Stenbit, A. E., Burcelin, R., Katz, E. B., Tsao, T. S., Gautier, N., Charron, M. J. and Le Marchand-Brustel, Y., 1996, Divers e effects of GLUT4 ablation on glucose uptake and glycogen synthesis in red and white skeletal muscle. Journal of Clinical Investigations, 98, 629 ± 634.
   PubMedGoogle Scholar
• Stenbit, A. E., Tsao, T. S., Li, J., Burcelin, R., Geenen, D. L., Factor, S. M., Hous eknecht, K., Katz, E. B. and Charron, M. J., 1997, GLUT4 heterozygous knockout mice develop muscle insulin resistance and diabetes. Nature Medicine, 10, 1096 ± 1101.
   Google Scholar
• Treadway, J. L., Hargrave, M. D., Nardone, N. A., McPherson, R. K., Russo, J. F., Milici, A. J., Stukenbrok, H. A., Gibbs, E. M., Stevenson, R. W. and Pessin, J. E., 1994, Enhanced peripheral glucose utilization in transgenic mice expressing the human GLUT4 gene. Journal of Biological Chemistry, 269, 29956 ± 29961.
   PubMed Web of Science ®Google Scholar
• Tsao, T. S., Burcelin, R., Katz, E. B., Huang, L. and Charron, M. J., 1996, Enhanced insulin action due to targeted GLUT4 over- expression exclusively in muscle. Diabetes, 45, 28 ± 36.
   Google Scholar
• Tsao, T. S., Katz, E. B., Pommer, D. and Charron, M. J., 2000, Amelioration of insulin resistance but not hyperinsulinemia in obes e mice overexpressing GLUT4 s electively in skeleta l muscle. Metabolism, 49, 340 ± 346.
   Google Scholar
• Tsao, T. S., Li, J., Chang, K. S., Stenbit, A. E., Galuska, D., Anderson, J. E., Zierath, J. R., McCarter, R. J. and Charron, M. J., 2001, Metabolic adaptations in skeletal muscle overexpressing GLUT4: effects on muscle and physical activity. FASEB Journal, 15, 958 ± 969.
   PubMed Web of Science ®Google Scholar
• Tsao, T.-S., Stenbit, A., Li, J., Houseknecht, K. L., Zierath, J. R., Katz, E. B. and Charron, M. J., 1997, Muscle-specific transgenic complementation of GLUT4-deficient mice: effects on glucose but not lipid metabolism. Journal of Clinical Investigations, 100, 671 ± 677.
   Google Scholar
• Vaag, A., Henriksen, J. E. and Beck-Niels en, H., 1992, Decreased insulin activation of glycogen synthas e in skeletal muscle in young nonobes e Caucasian first-degree relatives of patients with non- insulin-dependent diabetes mellitus. Journal of Clinical Investiga- tions, 89, 782 ± 788.
   Google Scholar
• Wallberg-Henriksson, H. and Holloszy, J. O., 1985, Activation of glucose transport in diabetic muscle: Responses to contraction and insulin. American Journal of Physiology (Cell Physiology), 249, C233 ± C237.
   Google Scholar
• Yeh, J.-I., Gulve, E. A., Rameh, L. and Birnbaum, M. J., 1995, The effects of wortmannin on rat skeletal muscle. Journal of Biologica l Chemistry, 270, 2107 ± 2111.
   PubMedGoogle Scholar
• Zierath, J. R., Galuska, D., Nolte, L., ThoÈrne, A., Smedegaard- Kristens en, J. and Wallberg-Henriksson, H., 1994, Effects of glycemia on glucos e transport in isolated skeletal muscle from patients with NIDDM: in vitro reversal of muscular insulin resistance. Diabetologia, 37, 270 ± 277.
   Google Scholar
• Zierath, J. R., Hous eknecht, K., Gnudi, L. and Kahn, B. B., 1997, High fat feeding impairs insulin-stimulated GLUT4 recruitment in muscle via an early insulin signaling defect. Diabetes, 46, 215 ± 223.
   Google Scholar
• Zierath, J. R., Tsao, T.-S., Stenbit, A. E., Ryder, J. W., Galuska, D. and Charron, M. J., 1998, Restoration of hypoxia-stimulated glucose uptake in GLUT4-deficient muscles by muscle-specific GLUT4 transgenic complementation. Journal of Biologica l Chem- istry, 273, 20910 ± 20915.
   PubMedGoogle Scholar
• Zisman, A., Peroni, O. D., Abel, E. D., Michael, M. D., Mauvais- Jarvis, F., Lowell, B. B., Wojtaszewski, J. F., Hirshman, M. F., Virkamaki, A., Goodyear, L. J., Kahn, C. R. and Kahn, B. B., 2000, Targeted disruption of the glucose transporter 4 s electively in muscle caus es insulin resistance and glucos e intolerance. Nature Medicine, 6, 924 ± 928.
   PubMed Web of Science ®Google Scholar