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ISRN Molecular Biology
Volume 2012 (2012), Article ID 856987, 12 pages
http://dx.doi.org/10.5402/2012/856987
Review Article

Regulation of GLUT4 and Insulin-Dependent Glucose Flux

Department of Biochemistry and Molecular Biology, University of Oklahoma Health Sciences Center, P.O. Box 26901, BMSB 964, Oklahoma City, OK 73190, USA

Received 2 September 2012; Accepted 24 September 2012

Academic Editors: A. M. Da Silva and H.-C. Lee

Copyright © 2012 Ann Louise Olson. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. D. R. Matthews, J. P. Hosker, and A. S. Rudenski, “Homeostasis model assessment: insulin resistance and β-cell function from fasting plasma glucose and insulin concentrations in man,” Diabetologia, vol. 28, no. 7, pp. 412–419, 1985. View at Scopus
  2. S. T. McCarthy, E. Harris, and R. C. Turner, “Glucose control of basal insulin secretion in diabetes,” Diabetologia, vol. 13, no. 2, pp. 93–97, 1977. View at Scopus
  3. A. B. Fernandes, R. S. Patarrao, P. A. Videira, and M. P. Macedo, “Understanding post-prandial glucose clearance by peripheral organs: the role of the hepatic parasympathetic system,” Journal of Neuroendocrinology, vol. 23, pp. 1288–1295, 2011. View at Publisher · View at Google Scholar
  4. B. Thorens, Z. Q. Cheng, D. Brown, and H. F. Lodish, “Liver glucose transporter: a basolateral protein in hepatocytes and intestine and kidney cells,” American Journal of Physiology, vol. 259, no. 2, pp. C279–C285, 1990. View at Scopus
  5. B. Thorens, H. K. Sarkar, H. R. Kaback, and H. F. Lodish, “Cloning and functional expression in bacteria of a novel glucose transporter present in liver, intestine, kidney, and β-pancreatic islet cells,” Cell, vol. 55, no. 2, pp. 281–290, 1988. View at Scopus
  6. J. Vinten, J. Gliemann, and K. Osterlind, “Exchange of 3-O-methylglucose in isolated fat cells,” Journal of Biological Chemistry, vol. 251, no. 3, pp. 794–800, 1976. View at Scopus
  7. S. W. Cushman and L. J. Wardzala, “Potential mechanism of insulin action on glucose transport in the isolated rat adipose cell,” Journal of Biological Chemistry, vol. 255, no. 10, pp. 4758–4762, 1980. View at Scopus
  8. K. Suzuki and T. Kono, “Evidence that insulin causes translocation of glucose transport activity to the plasma membrane from an intracellular storage site,” Proceedings of the National Academy of Sciences of the United States of America, vol. 77, no. 5 I, pp. 2542–2545, 1980. View at Scopus
  9. D. E. James, R. Brown, J. Navarro, and P. F. Pilch, “Insulin-regulatable tissues express a unique insulin-sensitive glucose transport protein,” Nature, vol. 333, no. 6169, pp. 183–185, 1988. View at Scopus
  10. M. J. Birnbaum, “Identification of a novel gene encoding an insulin-responsive glucose transporter protein,” Cell, vol. 57, no. 2, pp. 305–315, 1989. View at Scopus
  11. M. J. Charron, F. C. Brosius, S. L. Alper, and H. F. Lodish, “A glucose transport protein expressed predominately in insulin-responsive tissues,” Proceedings of the National Academy of Sciences of the United States of America, vol. 86, no. 8, pp. 2535–2539, 1989. View at Scopus
  12. D. E. James, M. Strube, and M. Mueckler, “Molecular cloning and characterization of an insulin-regulatable glucose transporter,” Nature, vol. 338, no. 6210, pp. 83–87, 1989. View at Scopus
  13. S. H. Purcell, L. B. Aerni-Flessner, A. R. Willcockson, K. A. Diggs-Andrews, S. J. Fisher, and K. H. Moley, “Improved insulin sensitivity by GLUT12 overexpression in mice,” Diabetes, vol. 60, no. 5, pp. 1478–1482, 2011. View at Publisher · View at Google Scholar · View at Scopus
  14. S. Rogers, M. L. Macheda, S. E. Docherty et al., “Identification of a novel glucose transporter-like protein—GLUT-12,” American Journal of Physiology, vol. 282, no. 3, pp. E733–E738, 2002. View at Scopus
  15. C. A. Stuart, M. E. A. Howell, Y. Zhang, and D. Yin, “Insulin-stimulated translocation of glucose transporter (GLUT) 12 parallels that of GLUT4 in normal muscle,” Journal of Clinical Endocrinology and Metabolism, vol. 94, no. 9, pp. 3535–3542, 2009. View at Publisher · View at Google Scholar · View at Scopus
  16. E. B. Katz, A. E. Stenbit, K. Hatton, R. DePinho, and M. J. Charron, “Cardiac and adipose tissue abnormalities but not diabetes in mice deficient in GLUT4,” Nature, vol. 377, no. 6545, pp. 151–155, 1995. View at Scopus
  17. C. A. Millar, T. Meerloo, S. Martin et al., “Adipsin and the glucose transporter GLUT4 traffic to the cell surface via independent pathways in adipocytes,” Traffic, vol. 1, no. 2, pp. 141–151, 2000. View at Scopus
  18. K. V. Kandror, L. Coderre, A. V. Pushkin, and P. F. Pilch, “Comparison of glucose-transporter-containing vesicles from rat fat and muscle tissues: evidence for a unique endosomal compartment,” Biochemical Journal, vol. 307, no. 2, pp. 383–390, 1995. View at Scopus
  19. S. Lund, G. D. Holman, O. Schmitz, and O. Pedersen, “Contraction stimulates translocation of glucose transporter GLUT4 in skeletal muscle through a mechanism distinct from that of insulin,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 13, pp. 5817–5821, 1995. View at Publisher · View at Google Scholar · View at Scopus
  20. J. W. Slot, H. J. Geuze, S. Gigengack, D. E. James, and G. E. Lienhard, “Translocation of the glucose transporter GLUT4 in cardiac myocytes of the rat,” Proceedings of the National Academy of Sciences of the United States of America, vol. 88, no. 17, pp. 7815–7819, 1991. View at Scopus
  21. J. W. Slot, H. J. Geuze, S. Gigengack, G. E. Lienhard, and D. E. James, “Immuno-localization of the insulin regulatable glucose transporter in brown adipose tissue of the rat,” Journal of Cell Biology, vol. 113, no. 1, pp. 123–135, 1991. View at Scopus
  22. C. Livingstone, D. E. James, J. E. Rice, D. Hanpeter, and G. W. Gould, “Compartment ablation analysis of the insulin-responsive glucose transporter (GLUT4) in 3T3-L1 adipocytes,” Biochemical Journal, vol. 315, no. 2, pp. 487–495, 1996. View at Scopus
  23. S. Martin, J. Tellam, C. Livingstone, J. W. Slot, G. W. Gould, and D. E. James, “The glucose transporter (GLUT-4) and vesicle-associated membrane protein-2 (VAMP-2) are segregated from recycling endosomes in insulin- sensitive cells,” Journal of Cell Biology, vol. 134, no. 3, pp. 625–635, 1996. View at Scopus
  24. A. K. El-Jack, K. V. Kandror, and P. F. Pilch, “The formation of an insulin-responsive vesicular cargo compartment is an early event in 3T3-L1 adipocyte differentiation,” Molecular Biology of the Cell, vol. 10, no. 5, pp. 1581–1594, 1999. View at Scopus
  25. H. Al-Hasani, C. S. Hinck, and S. W. Cushman, “Endocytosis of the glucose transporter GLUT4 is mediated by the GTPase dynamin,” Journal of Biological Chemistry, vol. 273, no. 28, pp. 17504–17510, 1998. View at Publisher · View at Google Scholar · View at Scopus
  26. D. Williams and J. E. Pessin, “Mapping of R-SNARE function at distinct intracellular GLUT4 trafficking steps in adipocytes,” Journal of Cell Biology, vol. 180, no. 2, pp. 375–387, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. M. A. Lampson, J. Schmoranzer, A. Zeigerer, S. M. Simon, and T. E. McGraw, “Insulin-regulated release from the endosomal recycling compartment is regulated by budding of specialized vesicles,” Molecular Biology of the Cell, vol. 12, no. 11, pp. 3489–3501, 2001. View at Scopus
  28. T. A. Kupriyanova, V. Kandror, and K. V. Kandror, “Isolation and characterization of the two major intracellular Glut4 storage compartments,” Journal of Biological Chemistry, vol. 277, no. 11, pp. 9133–9138, 2002. View at Publisher · View at Google Scholar · View at Scopus
  29. A. Zeigerer, M. A. Lampson, O. Karylowski et al., “GLUT4 retention in adipocytes requires two intracellular insulin-regulated transport steps,” Molecular Biology of the Cell, vol. 13, no. 7, pp. 2421–2435, 2002. View at Publisher · View at Google Scholar · View at Scopus
  30. A. M. Shewan, E. M. Van Dam, S. Martin et al., “GLUT4 recycles via a trans-Golgi network (TGN) subdomain enriched in Syntaxins 6 and 16 but not TGN38: involvement of an acidic targeting motif,” Molecular Biology of the Cell, vol. 14, no. 3, pp. 973–986, 2003. View at Publisher · View at Google Scholar · View at Scopus
  31. N. J. Bryant, R. Govers, and D. E. James, “Regulated transport of the glucose transporter GLUT4,” Nature Reviews Molecular Cell Biology, vol. 3, no. 4, pp. 267–277, 2002. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Hashiramoto and D. E. James, “Characterization of insulin-responsive GLUT4 storage vesicles isolated from 3T3-L1 adipocytes,” Molecular and Cellular Biology, vol. 20, no. 1, pp. 416–427, 2000. View at Scopus
  33. L. J. Robinson, S. Pang, D. S. Harris, J. Heuser, and D. E. James, “Translocation of the glucose transporter (GLUT4) to the cell surface in permeabilized 3T3-L1 adipocytes: effects of ATP, insulin, and GTPγS and localization of GLUT4 to clathrin lattices,” Journal of Cell Biology, vol. 117, no. 6, pp. 1181–1196, 1992. View at Publisher · View at Google Scholar · View at Scopus
  34. G. D. Holman, L. L. Leggio, and S. W. Cushman, “Insulin-stimulated GLUT4 glucose transporter recycling. A problem in membrane protein subcellular trafficking through multiple pools,” Journal of Biological Chemistry, vol. 269, no. 26, pp. 17516–17524, 1994. View at Scopus
  35. J. Yang and G. D. Holman, “Comparison of GLUT4 and GLUT1 subcellular trafficking in basal and insulin-stimulated 3T3-L1 cells,” Journal of Biological Chemistry, vol. 268, no. 7, pp. 4600–4603, 1993. View at Scopus
  36. M. P. Czech and J. M. Buxton, “Insulin action on the internalization of the GLUT4 glucose transporter in isolated rat adipocytes,” Journal of Biological Chemistry, vol. 268, no. 13, pp. 9187–9190, 1993. View at Scopus
  37. D. E. James, “MUNC-ing around with insulin action,” Journal of Clinical Investigation, vol. 115, no. 2, pp. 219–221, 2005. View at Publisher · View at Google Scholar · View at Scopus
  38. J. L. Jewell, E. Oh, L. Ramalingam et al., “Munc18c phosphorylation by the insulin receptor links cell signaling directly to SNARE exocytosis,” Journal of Cell Biology, vol. 193, no. 1, pp. 185–199, 2011. View at Publisher · View at Google Scholar · View at Scopus
  39. S. Semiz, J. G. Park, S. M. C. Nicoloro et al., “Conventional kinesin KIF5B mediates insulin-stimulated GLUT4 movements on microtubules,” EMBO Journal, vol. 22, no. 10, pp. 2387–2399, 2003. View at Publisher · View at Google Scholar · View at Scopus
  40. J. S. Bogan, N. Hendon, A. E. McKee, T. S. Tsao, and H. F. Lodish, “Functional cloning of TUG as a regulator of GLUT4 glucose transporter trafficking,” Nature, vol. 425, no. 6959, pp. 727–733, 2003. View at Publisher · View at Google Scholar · View at Scopus
  41. C. A. Eyster, Q. S. Duggins, G. J. Gorbsky, and A. L. Olson, “Microtubule network is required for insulin signaling through activation of Akt/protein kinase B: evidence that insulin stimulates vesicle docking/fusion but not intracellular mobility,” Journal of Biological Chemistry, vol. 281, no. 51, pp. 39719–39727, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. V. A. Lizunov, H. Matsumoto, J. Zimmerberg, S. W. Cushman, and V. A. Frolov, “Insulin stimulates the halting, tethering, and fusion of mobile GLUT4 vesicles in rat adipose cells,” Journal of Cell Biology, vol. 169, no. 3, pp. 481–489, 2005. View at Publisher · View at Google Scholar · View at Scopus
  43. S. Huang, L. M. Lifshitz, C. Jones et al., “Insulin stimulates membrane fusion and GLUT4 accumulation in clathrin coats on adipocyte plasma membranes,” Molecular and Cellular Biology, vol. 27, no. 9, pp. 3456–3469, 2007. View at Publisher · View at Google Scholar · View at Scopus
  44. L. Bai, Y. Wang, J. Fan et al., “Dissecting multiple steps of GLUT4 trafficking and identifying the sites of insulin action,” Cell Metabolism, vol. 5, no. 1, pp. 47–57, 2007. View at Publisher · View at Google Scholar · View at Scopus
  45. B. Cheatham and C. R. Kahn, “Insulin action and the insulin signaling network,” Endocrine Reviews, vol. 16, no. 2, pp. 117–142, 1995. View at Scopus
  46. M. F. White, “The IRS-signaling system: a network of docking proteins that mediate insulin and cytokine action,” Recent Progress in Hormone Research, vol. 53, pp. 119–138, 1998. View at Scopus
  47. L. Chang, S. H. Chiang, and A. R. Saltiel, “Insulin signaling and the regulation of glucose transport,” Molecular Medicine, vol. 10, no. 7-12, pp. 65–71, 2004. View at Publisher · View at Google Scholar · View at Scopus
  48. D. J. Withers, J. S. Gutierrez, H. Towery et al., “Disruption of IRS-2 causes type 2 diabetes in mice,” Nature, vol. 391, no. 6670, pp. 900–904, 1998. View at Publisher · View at Google Scholar · View at Scopus
  49. M. Fasshauer, J. Klein, K. Ueki et al., “Essential role of insulin receptor substrate-2 in insulin stimulation of Glut4 translocation and glucose uptake in brown adipocytes,” Journal of Biological Chemistry, vol. 275, no. 33, pp. 25494–25501, 2000. View at Publisher · View at Google Scholar · View at Scopus
  50. M. G. Myers Jr., L. M. Wang, X. J. Sun et al., “Role of IRS-1-GRB-2 complexes in insulin signaling,” Molecular and Cellular Biology, vol. 14, no. 6, pp. 3577–3587, 1994. View at Scopus
  51. J. M. Backer, J. M. G. Myers Jr., S. E. Shoelson et al., “Phosphatidylinositol 3'-kinase is activated by association with IRS-1 during insulin stimulation,” EMBO Journal, vol. 11, no. 9, pp. 3469–3479, 1992. View at Scopus
  52. A. R. Saltiel and C. R. Kahn, “Insulin signalling and the regulation of glucose and lipid metabolism,” Nature, vol. 414, no. 6865, pp. 799–806, 2001. View at Publisher · View at Google Scholar · View at Scopus
  53. G. I. Welsh, I. Hers, D. C. Berwick et al., “Role of protein kinase B in insulin-regulated glucose uptake,” Biochemical Society Transactions, vol. 33, no. 2, pp. 346–349, 2005. View at Publisher · View at Google Scholar · View at Scopus
  54. Q. I. Zhou, J. G. Park, Z. Y. Jiang et al., “Analysis of insulin signalling by RNAi-based gene silencing,” Biochemical Society Transactions, vol. 32, no. 5, pp. 817–821, 2004. View at Publisher · View at Google Scholar · View at Scopus
  55. S. Masure, B. Haefner, J. J. Wesselink et al., “Molecular cloning, expression and characterization of the human serine/threonine kinase Akt-3,” European Journal of Biochemistry, vol. 265, no. 1, pp. 353–360, 1999. View at Publisher · View at Google Scholar · View at Scopus
  56. A. D. Kohn, S. A. Summers, M. J. Birnbaum, and R. A. Roth, “Expression of a constitutively active Akt Ser/Thr kinase in 3T3-L1 adipocytes stimulates glucose uptake and glucose transporter 4 translocation,” Journal of Biological Chemistry, vol. 271, no. 49, pp. 31372–31378, 1996. View at Publisher · View at Google Scholar · View at Scopus
  57. H. Cho, J. Mu, J. K. Kim et al., “Insulin resistance and a diabetes mellitus-like syndrome in mice lacking the protein kinase Akt2 (PKBβ),” Science, vol. 292, no. 5522, pp. 1728–1731, 2001. View at Publisher · View at Google Scholar · View at Scopus
  58. M. P. Czech and S. Corvera, “Signaling mechanisms that regulate glucose transport,” Journal of Biological Chemistry, vol. 274, no. 4, pp. 1865–1868, 1999. View at Publisher · View at Google Scholar · View at Scopus
  59. T. Yamada, H. Katagiri, T. Asano et al., “Role of PDK1 in insulin-signaling pathway for glucose metabolism in 3T3-L1 adipocytes,” American Journal of Physiology. Endocrinology and Metabolism, vol. 282, no. 6, pp. E1385–E1394, 2002. View at Scopus
  60. L. Q. Dong and F. Liu, “PDK2: the missing piece in the receptor tyrosine kinase signaling pathway puzzle,” American Journal of Physiology. Endocrinology and Metabolism, vol. 289, no. 2, pp. E187–E196, 2005. View at Publisher · View at Google Scholar · View at Scopus
  61. D. D. Sarbassov, D. A. Guertin, S. M. Ali, and D. M. Sabatini, “Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex,” Science, vol. 307, no. 5712, pp. 1098–1101, 2005. View at Publisher · View at Google Scholar · View at Scopus
  62. R. C. Hresko and M. Mueckler, “mTOR·RICTOR is the Ser473 kinase for Akt/protein kinase B in 3T3-L1 adipocytes,” Journal of Biological Chemistry, vol. 280, no. 49, pp. 40406–40416, 2005. View at Publisher · View at Google Scholar · View at Scopus
  63. V. Zinzalla, D. Stracka, W. Oppliger, and M. N. Hall, “Activation of mTORC2 by association with the ribosome,” Cell, vol. 144, no. 5, pp. 757–768, 2011. View at Publisher · View at Google Scholar · View at Scopus
  64. R. C. Hresko, H. Murata, and M. Mueckler, “Phosphoinositide-dependent kinase-2 is a distinct protein kinase in a novel cytoskeletal fraction associated with adipocyte plasma membranes,” Journal of Biological Chemistry, vol. 278, no. 24, pp. 21615–21622, 2003. View at Publisher · View at Google Scholar · View at Scopus
  65. M. P. Scheid, P. A. Marignani, and J. R. Woodgett, “Multiple phosphoinositide 3-kinase-dependent steps in activation of protein kinase B,” Molecular and Cellular Biology, vol. 22, no. 17, pp. 6247–6260, 2002. View at Publisher · View at Google Scholar · View at Scopus
  66. A. Kumar, J. C. Lawrence Jr., D. Y. Jung et al., “Fat cell-specific ablation of rictor in mice impairs insulin-regulated fat cell and whole-body glucose and lipid metabolism,” Diabetes, vol. 59, no. 6, pp. 1397–1406, 2010. View at Publisher · View at Google Scholar · View at Scopus
  67. S. Kane, H. Sano, S. C. H. Liu et al., “A method to identify serine kinase substrates. Akt phosphorylates a novel adipocyte protein with a Rab GTPase-activating protein (GAP) domain,” Journal of Biological Chemistry, vol. 277, no. 25, pp. 22115–22118, 2002. View at Publisher · View at Google Scholar · View at Scopus
  68. M. Zerial and H. McBride, “Rab proteins as membrane organizers,” Nature Reviews Molecular Cell Biology, vol. 2, no. 2, pp. 107–117, 2001. View at Publisher · View at Google Scholar · View at Scopus
  69. H. Sano, S. Kane, E. Sano et al., “Insulin-stimulated phosphorylation of a Rab GTPase-activating protein regulates GLUT4 translocation,” Journal of Biological Chemistry, vol. 278, no. 17, pp. 14599–14602, 2003. View at Publisher · View at Google Scholar · View at Scopus
  70. M. Larance, G. Ramm, J. Stöckli et al., “Characterization of the role of the Rab GTPase-activating protein AS160 in insulin-regulated GLUT4 trafficking,” Journal of Biological Chemistry, vol. 280, no. 45, pp. 37803–37813, 2005. View at Publisher · View at Google Scholar · View at Scopus
  71. H. Sano, L. Eguez, M. N. Teruel et al., “Rab10, a target of the AS160 Rab GAP, is required for insulin-stimulated translocation of GLUT4 to the adipocyte plasma membrane,” Cell Metabolism, vol. 5, no. 4, pp. 293–303, 2007. View at Publisher · View at Google Scholar · View at Scopus
  72. H. Sano, W. G. Roach, G. R. Peck, M. Fukuda, and G. E. Lienhard, “Rab10 in insulin-stimulated GLUT4 translocation,” Biochemical Journal, vol. 411, no. 1, pp. 89–95, 2008. View at Publisher · View at Google Scholar · View at Scopus
  73. Y. Chen, Y. Wang, J. Zhang et al., “Rab10 and myosin-Va mediate insulin-stimulated GLUT4 storage vesicle trasnlocation in adipocytes,” The Journal of Cell Biology, vol. 198, pp. 545–560, 2012. View at Publisher · View at Google Scholar
  74. D. H. Wasserman, L. Kang, J. E. Ayala, P. T. Fueger, and R. S. Lee-Young, “The physiological regulation of glucose flux into muscle in vivo,” Journal of Experimental Biology, vol. 214, no. 2, pp. 254–262, 2011. View at Publisher · View at Google Scholar · View at Scopus
  75. R. M. O'Doherty, D. P. Bracy, H. Osawa, D. H. Wasserman, and D. K. Granner, “Rat skeletal muscle hexokinase II mRNA and activity are increased by a single bout of acute exercise,” American Journal of Physiology, vol. 266, no. 2, pp. E171–E178, 1994. View at Scopus
  76. P. T. Fueger, H. S. Hess, K. A. Posey et al., “Control of exercise-stimulated muscle glucose uptake by GLUT4 is dependent on glucose phosphorylation capacity in the conscious mouse,” Journal of Biological Chemistry, vol. 279, no. 49, pp. 50956–50961, 2004. View at Publisher · View at Google Scholar · View at Scopus
  77. M. L. Liu, E. M. Gibbs, S. C. McCoid et al., “Transgenic mice expressing the human GLUT4/muscle-fat facilitative glucose transporter protein exhibit efficient glycemic control,” Proceedings of the National Academy of Sciences of the United States of America, vol. 90, no. 23, pp. 11346–11350, 1993. View at Publisher · View at Google Scholar · View at Scopus
  78. P. R. Shepherd, L. Gnudi, E. Tozzo, H. Yang, F. Leach, and B. B. Kahn, “Adipose cell hyperplasia and enhanced glucose disposal in transgenic mice overexpressing GLUT4 selectively in adipose tissue,” Journal of Biological Chemistry, vol. 268, no. 30, pp. 22243–22246, 1993. View at Scopus
  79. T. S. Tsao, A. E. Stenbit, J. Li et al., “Muscle-specific transgenic complementation of GLUT4-deficient mice: effects on glucose but not lipid metabolism,” Journal of Clinical Investigation, vol. 100, no. 3, pp. 671–677, 1997. View at Scopus
  80. E. D. Abel, H. C. Kaulbach, R. Tian et al., “Cardiac hypertrophy with preserved contractile function after selective deletion of GLUT4 from the heart,” Journal of Clinical Investigation, vol. 104, no. 12, pp. 1703–1714, 1999. View at Scopus
  81. E. B. Katz, A. E. Stenbit, K. Hatton, R. DePinho, and M. J. Charron, “Cardiac and adipose tissue abnormalities but not diabetes in mice deficient in GLUT4,” Nature, vol. 377, no. 6545, pp. 151–155, 1995. View at Scopus
  82. Y. Li, A. R. Wende, O. Nunthakungwan et al., “Cytosolic, but not mitochondrial, oxidative stress is a likely contributer to cardiac hypertrophy resulting form cardiac specific GLUT4 deletion in mice,” FEBS Journal, vol. 279, pp. 599–611, 2012.
  83. S. Ikemoto, K. S. Thompson, M. Takahashi, H. Itakura, M. D. Lane, and O. Ezaki, “High fat diet-induced hyperglycemia: prevention by low level expression of a glucose transporter (GLUT4) minigene in transgenic mice,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 8, pp. 3096–3099, 1995. View at Scopus
  84. W. T. Garvey, L. Maianu, T. P. Huecksteadt, M. J. Birnbaum, J. M. Molina, and T. P. Ciaraldi, “Pretranslational suppression of a glucose transporter protein causes insulin resistance in adipocytes from patients with non-insulin-dependent diabetes mellitus and obesity,” Journal of Clinical Investigation, vol. 87, no. 3, pp. 1072–1081, 1991. View at Scopus
  85. J. Berger, C. Biswas, P. P. Vicario, H. V. Strout, R. Saperstein, and P. F. Pilch, “Decreased expression of the insulin-responsive glucose transporter in diabetes and fasting,” Nature, vol. 340, no. 6228, pp. 70–72, 1989. View at Scopus
  86. S. W. Cushman and L. J. Wardzala, “Potential mechanism of insulin action on glucose transport in the isolated rat adipose cell. Apparent translocation of intracellular transport systems to the plasma membrane,” Journal of Biological Chemistry, vol. 255, no. 10, pp. 4758–4762, 1980. View at Scopus
  87. W. I. Sivitz, S. L. DeSautel, T. Kayano, G. I. Bell, and J. E. Pessin, “Regulation of glucose transporter messenger RNA in insulin-deficient states,” Nature, vol. 340, no. 6228, pp. 72–74, 1989. View at Scopus
  88. E. D. Abel, O. Peroni, J. K. Kim et al., “Adipose-selective targeting of the GLUT4 gene impairs insulin action in muscle and liver,” Nature, vol. 409, no. 6821, pp. 729–733, 2001. View at Publisher · View at Google Scholar · View at Scopus
  89. R. A. De Fronzo, E. Jacot, E. Jequier, E. Maeder, J. Wahren, and J. P. Felber, “The effect of insulin on the disposal of intravenous glucose. Results from indirect calorimetry and hepatic and femoral venous catheterization,” Diabetes, vol. 30, no. 12, pp. 1000–1007, 1981. View at Scopus
  90. J. L. Treadway, D. M. Hargrove, N. A. Nardone et al., “Enhanced peripheral glucose utilization in transgenic mice expressing the human GLUT4 gene,” Journal of Biological Chemistry, vol. 269, no. 47, pp. 29956–29961, 1994. View at Scopus
  91. A. Zisman, O. D. Peroni, E. D. Abel et al., “Targeted disruption of the glucose transporter 4 selectively in muscle causes insulin resistance and glucose intolerance,” Nature Medicine, vol. 6, no. 8, pp. 924–928, 2000. View at Publisher · View at Google Scholar · View at Scopus
  92. C. B. Hollenbeck, Y. D. I. Chen, and G. M. Reaven, “A comparison of the relative effects of obesity and non-insulin-dependent diabetes mellitus on in vivo insulin-stimulated glucose utilization,” Diabetes, vol. 33, no. 7, pp. 622–626, 1984. View at Scopus
  93. M. Pendergrass, A. Bertoldo, R. Bonadonna et al., “Muscle glucose transport and phosphorylation in type 2 diabetic, obese nondiabetic, and genetically predisposed individuals,” American Journal of Physiology. Endocrinology and Metabolism, vol. 292, no. 1, pp. E92–E100, 2007. View at Publisher · View at Google Scholar · View at Scopus
  94. B. B. Kahn, “Dietary regulation of glucose transporter gene expression: tissue specific effects in adipose cells and muscle,” Journal of Nutrition, vol. 124, no. 8, pp. 1289S–1295S, 1994. View at Scopus
  95. P. A. Hansen, D. H. Han, B. A. Marshall et al., “A high fat diet impairs stimulation of glucose transport in muscle: functional evaluation of potential mechanisms,” Journal of Biological Chemistry, vol. 273, no. 40, pp. 26157–26163, 1998. View at Publisher · View at Google Scholar · View at Scopus
  96. J. O. Holloszy, “Regulation by exercise of skeletal muscle content of mitochondria and GLUT4,” Journal of Physiology and Pharmacology, vol. 59, no. 7, pp. 5–18, 2008. View at Scopus
  97. J. R. Zierath, T. S. Tsao, A. E. Stenbit, J. W. Ryder, D. Galuska, and M. J. Charron, “Restoration of hypoxia-stimulated glucose uptake in GLUT4-deficient muscles by muscle-specific GLUT4 transgenic complementation,” Journal of Biological Chemistry, vol. 273, no. 33, pp. 20910–20915, 1998. View at Publisher · View at Google Scholar · View at Scopus
  98. J. W. Ryder, Y. Kawano, D. Galuska et al., “Postexercise glucose uptake and glycogen synthesis in skeletal muscle from GLUT4-deficient mice,” FASEB Journal, vol. 13, no. 15, pp. 2246–2256, 1999. View at Scopus
  99. A. Leturque, M. Loizeau, S. Vaulont, M. Salminen, and J. Girard, “Improvement of insulin action in diabetic transgenic mice selectively overexpressing GLUT4 in skeletal muscle,” Diabetes, vol. 45, no. 1, pp. 23–27, 1996. View at Scopus
  100. J. T. Brozinick, S. C. McCoid, T. H. Reynolds et al., “GLUT4 overexpression in db/db mice dose-dependently ameliorates diabetes but is not a lifelong cure,” Diabetes, vol. 50, no. 3, pp. 593–600, 2001. View at Scopus
  101. B. A. Marshall, P. A. Hansen, N. J. Ensor, M. A. Ogden, and M. Mueckler, “GLUT-1 or GLUT-4 transgenes in obese mice improve glucose tolerance but do not prevent insulin resistance,” American Journal of Physiology. Endocrinology and Metabolism, vol. 276, no. 2, pp. E390–E400, 1999. View at Scopus
  102. L. M. Semeniuk, A. J. Kryski, and D. L. Severson, “Echocardiographic assessment of cardiac function in diabetic db/db and transgenic db/db-hGLUT4 mice,” American Journal of Physiology. Heart and Circulatory Physiology, vol. 283, no. 3, pp. H976–H982, 2002. View at Scopus
  103. E. Tozzo, L. Gnudi, and B. B. Kahn, “Amelioration of insulin resistance in streptozotocin diabetic mice by transgenic overexpression of GLUT4 driven by an adipose-specific promoter,” Endocrinology, vol. 138, no. 4, pp. 1604–1611, 1997. View at Publisher · View at Google Scholar · View at Scopus
  104. L. Gnudi, D. R. Jensen, E. Tozzo, R. H. Eckel, and B. B. Kahn, “Adipose-specific overexpression of GLUT-4 in transgenic mice alters lipoprotein lipase activity,” American Journal of Physiology. Regulatory Integrative and Comparative Physiology, vol. 270, no. 4, pp. R785–R792, 1996. View at Scopus
  105. T. S. Tsao, R. Burcelin, E. B. Katz, L. Huang, and M. J. Charron, “Enhanced insulin action due to targeted GLUT4 overexpression exclusively in muscle,” Diabetes, vol. 45, no. 1, pp. 28–36, 1996. View at Scopus
  106. M. A. Herman, O. D. Peroni, J. Villoria et al., “A novel ChREBP isoform in adipose tissue regulates systemic glucose metabolism,” Nature, vol. 484, pp. 333–340, 2012. View at Publisher · View at Google Scholar
  107. A. L. Olson, M.-L. Liu, W. S. Moye-Rowley, J. B. Buse, G. I. Bell, and J. E. Pessin, “Hormonal/metabolic regulation of the human GLUT4/muscle-fat facilitative glucose transporter gene in transgenic mice,” Journal of Biological Chemistry, vol. 268, no. 13, pp. 9839–9846, 1993. View at Scopus
  108. L. J. Goodyear, M. F. Hirshman, P. M. Valyou, and E. S. Horton, “Glucose transporter number, function, and subcellular distribution in rat skeletal muscle after exercise training,” Diabetes, vol. 41, no. 9, pp. 1091–1099, 1992. View at Scopus
  109. P. D. Neufer, M. H. Shinebarger, and G. L. Dohm, “Effect of training and detraining on skeletal muscle glucose transporter (GLUT4) content in rats,” Canadian Journal of Physiology and Pharmacology, vol. 70, no. 9, pp. 1286–1290, 1992. View at Scopus
  110. K. J. Rodnick, E. J. Henriksen, D. E. James, and J. O. Holloszy, “Exercise training, glucose transporters, and glucose transport in rat skeletal muscles,” American Journal of Physiology. Cell Physiology, vol. 262, no. 1, pp. C9–C14, 1992. View at Scopus
  111. K. F. Petersen, S. Dufour, D. Befroy, M. Lehrke, R. E. Hendler, and G. I. Shulman, “Reversal of nonalcoholic hepatic steatosis, hepatic insulin resistance, and hyperglycemia by moderate weight reduction in patients with type 2 diabetes,” Diabetes, vol. 54, no. 3, pp. 603–608, 2005. View at Publisher · View at Google Scholar · View at Scopus
  112. E. M. Gibbs, J. L. Stock, S. C. McCoid et al., “Glycemic improvement in diabetic db/db mice by overexpression of the human insulin-regulatable glucose transporter (GLUT4),” Journal of Clinical Investigation, vol. 95, no. 4, pp. 1512–1518, 1995. View at Scopus
  113. T. Santalucia, M. Camps, A. Castello et al., “Developmental regulation of GLUT-1 (erythroid/Hep G2) and GLUT-4 (muscle/fat) glucose transporter expression in rat heart, skeletal muscle, and brown adipose tissue,” Endocrinology, vol. 130, no. 2, pp. 837–846, 1992. View at Publisher · View at Google Scholar · View at Scopus
  114. A. L. Olson, “Regulated of GLUT4 transcription and gene expression,” Current Medicinal Chemistry. Immunology, Endocrine & Metabolic Agents, vol. 5, pp. 219–225, 2005. View at Publisher · View at Google Scholar
  115. A. L. Olson and J. B. Knight, “Regulation of GLUT4 expression in vivo and in vitro,” Frontiers in Bioscience, vol. 8, pp. s401–s409, 2003. View at Scopus
  116. J. M. Richardson, T. W. Balon, J. L. Treadway, and J. E. Pessin, “Differential regulation of glucose transporter activity and expression in red and white skeletal muscle,” Journal of Biological Chemistry, vol. 266, no. 19, pp. 12690–12694, 1991. View at Scopus
  117. M. J. Charron and B. B. Kahn, “Divergent molecular mechanisms for insulin-resistant glucose transport in muscle and adipose cells in vivo,” Journal of Biological Chemistry, vol. 265, no. 14, pp. 7994–8000, 1990. View at Scopus
  118. P. M. Gerrits, A. L. Olson, and J. E. Pessin, “Regulation of the GLUT4/muscle-fat glucose transporter mRNA in adipose tissue of insulin-deficient diabetic rats,” Journal of Biological Chemistry, vol. 268, no. 1, pp. 640–644, 1993. View at Scopus
  119. P. D. Neufer, J. O. Carey, and G. L. Dohm, “Transcriptional regulation of the gene for glucose transporter GLUT4 in skeletal muscle. Effects of diabetes and fasting,” Journal of Biological Chemistry, vol. 268, no. 19, pp. 13824–13829, 1993. View at Scopus
  120. J. M. Ren, C. F. Semenkovich, E. A. Gulve, J. Gao, and J. O. Holloszy, “Exercise induces rapid increases in GLUT4 expression, glucose transport capacity, and insulin-stimulated glycogen storage in muscle,” Journal of Biological Chemistry, vol. 269, no. 20, pp. 14396–14401, 1994. View at Scopus
  121. K. Kawanaka, I. Tabata, S. Katsuta, and M. Higuchi, “Changes in insulin-stimulated glucose transport and GLUT-4 protein in rat skeletal muscle after training,” Journal of Applied Physiology, vol. 83, no. 6, pp. 2043–2047, 1997. View at Scopus
  122. H. H. Host, P. A. Hansen, L. A. Nolte, M. M. Chen, and J. O. Holloszy, “Rapid reversal of adaptive increases in muscle GLUT-4 and glucose transport capacity after training cessation,” Journal of Applied Physiology, vol. 84, no. 3, pp. 798–802, 1998. View at Scopus
  123. B. F. Holmes, D. B. Lang, M. J. Birnbaum, J. Mu, and G. L. Dohm, “AMP kinase is not required for the GLUT4 response to exercise and denervation in skeletal muscle,” American Journal of Physiology. Endocrinology and Metabolism, vol. 287, no. 4, pp. E739–E743, 2004. View at Publisher · View at Google Scholar · View at Scopus
  124. J. R. Flores-Riveros, K. H. Kaestner, K. S. Thompson, and M. D. Lane, “Cyclic AMP-induced transcription repression of the insulin-responsive glucose transporter (GLUT4) gene: identification of a promoter region required for down-regulation of transcription,” Biochemical and Biophysical Research Communications, vol. 194, no. 3, pp. 1148–1154, 1993. View at Publisher · View at Google Scholar · View at Scopus
  125. D. M. Calderhead, K. Kitagawa, L. I. Tanner, G. D. Holman, and G. E. Lienhard, “Insulin regulation of the two glucose transporters in 3T3-L1 adipocytes,” Journal of Biological Chemistry, vol. 265, no. 23, pp. 13800–13808, 1990. View at Scopus
  126. A. Garcia De Herreros and M. J. Birnbaum, “The regulation by insulin of glucose transporter gene expression in 3T3 adipocytes,” Journal of Biological Chemistry, vol. 264, no. 17, pp. 9885–9890, 1989. View at Scopus
  127. Y. Mitsumoto and A. Klip, “Developmental regulation of the subcellular distribution and glycosylation of GLUT1 and GLUT4 glucose transporters during myogenesis of L6 muscle cells,” Journal of Biological Chemistry, vol. 267, no. 7, pp. 4957–4962, 1992. View at Scopus
  128. M. L. Liu, A. L. Olson, N. P. Edgington, W. S. Moye-Rowley, and J. E. Pessin, “Myocyte enhancer factor 2 (MEF2) binding site is essential for C2C12 myotube-specific expression of the rat GLUT4/muscle-adipose facilitative glucose transporter gene,” Journal of Biological Chemistry, vol. 269, no. 45, pp. 28514–28521, 1994. View at Scopus
  129. J. M. Richardson and J. E. Pessin, “Identification of a skeletal muscle-specific regulatory domain in the rat GLUT4/muscle-fat gene,” Journal of Biological Chemistry, vol. 268, no. 28, pp. 21021–21027, 1993. View at Scopus
  130. J. B. Knight, C. A. Eyster, B. A. Griesel, and A. L. Olson, “Regulation of the human GLUT4 gene promoter: interaction between a transcriptional activator and myocyte enhancer factor 2A,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 25, pp. 14725–14730, 2003. View at Publisher · View at Google Scholar · View at Scopus
  131. D. W. Cooke and M. D. Lane, “A sequence element in the GLUT4 gene that mediates repression by insulin,” Journal of Biological Chemistry, vol. 273, no. 11, pp. 6210–6217, 1998. View at Publisher · View at Google Scholar · View at Scopus
  132. D. P. Sparling, B. A. Griesel, J. Weems, and A. L. Olson, “GLUT4 Enhancer Factor (GEF) interacts with MEF2A and HDAC5 to regulate the GLUT4 promoter in adipocytes,” Journal of Biological Chemistry, vol. 283, no. 12, pp. 7429–7437, 2008. View at Publisher · View at Google Scholar · View at Scopus
  133. J. Weems and A. L. Olson, “Class II histone deacetylases limit GLUT4 gene expression during adipocyte differentiation,” Journal of Biological Chemistry, vol. 286, no. 1, pp. 460–468, 2011. View at Publisher · View at Google Scholar · View at Scopus
  134. M. L. Liu, A. L. Olson, W. S. Moye-Rowley, J. B. Buse, G. I. Bell, and J. E. Pessin, “Expression and regulation of the human GLUT4/muscle-fat facilitative glucose transporter gene in transgenic mice,” Journal of Biological Chemistry, vol. 267, no. 17, pp. 11673–11676, 1992. View at Scopus
  135. M. V. Thai, S. Guruswamy, K. T. Cao, J. E. Pessin, and A. L. Olson, “Myocyte enhancer factor 2 (MEF2)-binding site is required for GLUT4 gene expression in transgenic mice: regulation of MEF2 DNA binding activity in insulin-deficient diabetes,” Journal of Biological Chemistry, vol. 273, no. 23, pp. 14285–14292, 1998. View at Publisher · View at Google Scholar · View at Scopus
  136. A. L. Olson, N. P. Edgington, W. S. Moye-Rowley, and J. E. Pessin, “Characterization of 5'-heterogeneity of the rat GLUT4/muscle-adipose glucose transporter gene product,” Endocrinology, vol. 136, no. 5, pp. 1962–1968, 1995. View at Scopus
  137. A. L. Olson and J. E. Pessin, “Transcriptional regulation of the human GLUT4 gene promoter in diabetic transgenic mice,” Journal of Biological Chemistry, vol. 270, no. 40, pp. 23491–23495, 1995. View at Publisher · View at Google Scholar · View at Scopus
  138. K. M. Oshel, J. B. Knight, K. T. Cao, M. V. Thai, and A. L. Olson, “Identification of a 30-base pair regulatory element and novel DNA binding protein that regulates the human GLUT4 promoter in transgenic mice,” Journal of Biological Chemistry, vol. 275, no. 31, pp. 23666–23673, 2000. View at Publisher · View at Google Scholar · View at Scopus
  139. D. P. Sparling, B. A. Griesel, and A. L. Olson, “Hyperphosphorylation of MEF2A in primary adipocytes correlates with downregulation of human GLUT4 gene promoter activity,” American Journal of Physiology. Endocrinology and Metabolism, vol. 292, no. 4, pp. E1149–E1156, 2007. View at Publisher · View at Google Scholar · View at Scopus
  140. S. L. McGee, D. Sparling, A. L. Olson, and M. Hargreaves, “Exercise increases MEF2- and GEF DNA-binding activity in human skeletal muscle,” FASEB Journal, vol. 20, no. 2, pp. 348–349, 2006. View at Publisher · View at Google Scholar · View at Scopus
  141. S. L. McGee, B. J. W. Van Denderen, K. F. Howlett et al., “AMP-activated protein kinase regulates GLUT4 transcription by phosphorylating histone deacetylase 5,” Diabetes, vol. 57, no. 4, pp. 860–867, 2008. View at Publisher · View at Google Scholar · View at Scopus
  142. S. L. McGee, E. Fairlie, A. P. Garnham, and M. Hargreaves, “Exercise-induced histone modifications in human skeletal muscle,” Journal of Physiology, vol. 587, no. 24, pp. 5951–5958, 2009. View at Publisher · View at Google Scholar · View at Scopus
  143. J. C. Weems, B. A. Griesel, and A. L. Olson, “Class II histone deacetylases downregulate GLUT4 transcription in response to increased cAMP signaling in cultured adipocytes and fasting mice,” Diabetes, vol. 61, pp. 1404–1414, 2012. View at Publisher · View at Google Scholar