The role of skeletal muscle glycogen breakdown for regulation of insulin sensitivity by exercise

Frontiers in Physiology

Volumn 2 DEC, Issue , 2011, Pages

  Jensen, Jørgen ^a   Rustad, Per Inge ^a   Kolnes, Anders Jensen ^b   Lai, Yu Chiang ^c  

^a NORWEGIAN SCHOOL OF SPORT SCIENCES   (Norway)

^b CHARLES UNIVERSITY   (Czech Republic)

^c DE DUVE INSTITUTE   (Belgium)

Author keywords

De novo lipogenesis; Exercise; Glycogen phosphorylase; Glycogen synthase; Insulin resistance; Type 2 diabetes

Indexed keywords

EID: 84861857806     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2011.00112     Document Type: Review

References (131)

1. Aas, V., Rokling-Andersen, M., Wen-saas, A. J., Thoresen, G. H., Kase, E. T., and Rustan, A. C. (2005). Lipid metabolism in human skeletal muscle cells: effects of palmitate and chronic hyperglycaemia. Acta Physiol. Scand. 183, 31-41.
2. Acheson, K. J., Schutz, Y., Bessard, T., Anantharaman, K., Flatt, J. P., and Jequier, E. (1988). Glycogen storage capacity and de novo lipogenesis during massive carbohydrate overfeeding in man. Am. J. Clin. Nutr. 48, 240-247.
3. Alessi, D. R., and Cohen, P. (1998). Mechanism of activation and function of protein kinase B. Curr. Opin. Genet. Dev. 8, 55-62.
4. Arias, E. B., Kim, J., Funai, K., and Cartee, G. D. (2007). Prior exercise increases phosphorylation of Akt substrate of 160 kDa (AS160) in rat skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 292, E1191-E1200.
5. Aslesen, R., Engebretsen, E. M. L., Franch, J., and Jensen, J. (2001). Glucose uptake and metabolic stress in rat muscles stimulated electrically with different protocols. J. Appl. Physiol. 91, 1237-1244.
6. Aslesen, R., and Jensen, J. (1998). Effects of epinephrine on glucose metabolism in contracting rat skeletal muscle. Am. J. Physiol. 275, E448-E456.
7. Åstrand, P. O., and Rodahl, K. (1992). Textbook of Work Physiology. New York: McGraw-Hill Book Company, 1-681.
8. Bergström, J., Hermansen, L., Hultman, E., and Saltin, B. (1967). Diet, muscle glycogen and physical performance. Acta Physiol. Scand. 71, 140-150.
9. Bergström, J., and Hultman, E. (1966). Muscle glycogen synthesis after exercise: an enhancing factor localized to the muscle cells in man. Nature 210, 319-310.
10. Betts, J. A., and Williams, C. (2010). Short-term recovery from prolonged exercise: exploring the potential for protein ingestion to accentuate the benefits of carbohydrate supplements. Sports Med. 40, 941-959.
11. Boushel, R., Gnaiger, E., Calbet, J. A., Gonzalez-Alonso, J.,Wright-Paradis, C., Sondergaard, H., Ara, I., Helge, J. W., and Saltin, B. (2011). Muscle mitochondrial capacity exceeds maximal oxygen delivery in humans. Mitochondrion 11, 303-307.
12. Bouskila, M., Hirshman, M. F., Jensen, J., Goodyear, L. J., and Sakamoto, K. (2008). Insulin promotes glycogen synthesis in the absence of GSK3 phosphorylation in skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 294, E28-E35.
13. Bouskila, M., Hunter, R. W., Ibrahim, A. F., Delattre, L., Peggie, M., van Diepen, J. A., Voshol, P. J., Jensen, J., and Sakamoto, K. (2010). Allosteric regulation of glycogen synthase controls glycogen synthesis in muscle. Cell Metab. 12, 456-466.
14. Brady, M. J. (2010). Allosteric trumps covalent in the control of glycogen synthesis. Cell Metab. 12, 428-430.
15. Bruce, C. R., Anderson, M. J., Carey, A. L., Newman, D. G., Bonen, A., Kriketos, A. D., Cooney, G. J., and Hawley, J. A. (2003). Muscle oxidative capacity is a better predictor of insulin sensitivity than lipid status. J. Clin. Endocrinol. Metab. 88, 5444-5451.
16. Burgomaster, K. A., Howarth, K. R., Phillips, S. M., Rakobowchuk, M., Macdonald, M. J., McGee, S. L., and Gibala, M. J. (2008). Similar metabolic adaptations during exercise after low volume sprint interval and traditional endurance training in humans. J. Physiol. (Lond.) 586, 151-160.
17. Burgomaster, K. A., Hughes, S. C., Heigenhauser, G. J., Bradwell, S. N., and Gibala, M. J. (2005). Six sessions of sprint interval training increases muscle oxidative potential and cycle endurance capacity in humans. J. Appl. Physiol. 98, 1985-1990.
18. Cartee, G. D., Young, D. A., Sleeper, M. D., Zierath, J., Wallberg-Henriksson, H., and Holloszy, J. O. (1989). Prolonged increase in insulin-stimilated glucose transport in muscle after exercise. Am. J. Physiol. 256, E494-E499.
19. Chasiotis, D., Sahlin, K., and Hultman, E. (1983). Regulation of glycogenolysis in human muscle in response to epinephrine infusion. J. Appl. Physiol. 54, 45-50.
20. Christ, C. Y., Hunt, D., Hancock, J., Garcia-Macedo, R., Mandarino, L. J., and Ivy, J. L. (2002). Exercise training improves muscle insulin resistance but not insulin receptor signaling in obese Zucker rats. J. Appl. Physiol. 92, 736-744.
21. Christ-Roberts, C. Y., Pratipanawatr, T., Pratipanawatr, W., Berria, R., Belfort, R., Kashyap, S., and Man-darino, L. J. (2004). Exercise training increases glycogen synthase activity and GLUT4 expression but not insulin signaling in overweight nondiabetic and type 2 diabetic subjects. Metabolism 53, 1233-1242.
22. Cleasby, M. E., Reinten, T. A., Cooney, G. J., James, D. E., and Kraegen, E. W. (2007). Functional studies of Akt isoform specificity in skeletal muscle in vivo; maintained insulin sensitivity despite reduced insulin receptor substrate-1 expression. Mol. Endocrinol. 21, 215-228.
23. Cohen, P. (1993). Dissection of the protein phosphorylation cascades involved in insulin and growth factor action. Biochem. Soc. Trans. 214, 555-567.
24. Cohen, P. (2002). The origins of protein phosphorylation. Nat. Cell Biol. 4, E127-E130.
25. Connett, R. J., and Sahlin, K. (1996). "Control of glycolysis and glycogen metabolism," in Handbook of Physiology. Exercise: Regulation and Integration of Multiple System, eds L. B. Rowell and J. T. Shepherd (Bethesda, MD: American Physiological Society), 870-911.
26. Cori, C. F., and Cori, G. T. (1928). The mechanism of epinephrine action. I. The influence of epinephrine on the carbohydrate metabolism of fasting rats, with a note on new formation of carbohydrates. J. Biol. Chem. 79, 309-319.
27. Costill, D. L., Sherman, W. M., Fink, W. J., Maresh, C.,Witten, M., and Miller, J. M. (1981). The role of dietary carbohydrates in muscle glycogen resynthesis after strenuous running. Am. J. Clin. Nutr. 34, 1831-1836.
28. Coyle, E. F., Coggan, A. R., Hemmert, M. K., and Ivy, J. L. (1986). Muscle glycogen utilization during prolonged strenuous exercise when fed carbohydrate. J. Appl. Physiol. 61, 165-172.
29. Danforth, W. H. (1965). Glycogen synthase activity in skeletal muscle. J. Biol. Chem. 240, 588-593.
30. Defronzo, R. A., Ferrannini, E., Sato, Y., Felig,P.,and Wahren, J. (1981a). Synergistic interaction between exercise and insulin on peripheral glucose uptake. J. Clin. Invest. 68, 1468-1474.
31. Defronzo, R. A., Jacot, E., Jequier, E., Maeder, E., Wahren, J., and Felber, J. P. (1981b). The effect of insulin on the disposal of intravenous glucose. Results from indirect calorimetry and hepatic and femoral venous catheterization. Diabetes 30, 1000-1007.
32. Dela, F., Handberg, A., Mikines, K. J., Vinten, J., and Galbo, H. (1993). GLUT 4 and insulin receptor binding and kinase activity in trained human muscle. J. Physiol. (Lond.) 469, 615-624.
33. Derave, W., Hansen, B. F., Lund, S., Kristiansen, S., and Richter, E. A. (2000). Muscle glycogen content affects insulin-stimulated glucose transport and protein kinase B activity. Am. J. Physiol. 279, E947-E955.
34. Derave, W., Lund, S., Holman, G. D., Wojtaszewski, J., Pedersen, O., and Richter, E. A. (1999). Contraction-stimulated muscle glucose transport and GLUT-4 surface content are dependent on glycogen concentration. Am. J. Physiol. 277, E1103-E1110.
35. Esbjornsson-Liljedahl, M., Bodin, K., and Jansson, E. (2002). Smaller muscle ATP reduction in women than in men by repeated bouts of sprint exercise. J. Appl. Physiol. 93, 1075-1083.
36. Esbjornsson-Liljedahl, M., Sundberg, C. J., Norman, B., and Jansson, E. (1999). Metabolic response in type I and type II muscle fibers during a 30-s cycle sprint in men and women. J. Appl. Physiol. 87, 1326-1332.
37. Etgen, G. J., Jensen, J., Wilson, C. M., Hunt, D. G., Cushman, S. W., and Ivy, J. L. (1997). Exercise training reverses insulin resistance in muscle by enhanced recruitment of GLUT-4 to the cell surface. Am. J. Physiol. 272, E864-E869.
38. Etgen, G. J., Wilson, C. M., Jensen, J., Cushman,S.W.,and Ivy,J. L. (1996). Glucose transport and cell surface GLUT-4 protein in skeletal muscle of the obese Zucker rat. Am. J. Physiol. 271, E294-E301.
39. Franch, J., Aslesen, R., and Jensen, J. (1999). Regulation of glycogen synthesis in rat skeletal muscle after glycogen depleting contractile activity: effects of adrenaline on glycogen synthesis and activation of glycogen synthase and glycogen phosphorylase. Biochem. J. 344, 231-235.
40. Franch, J., Knudsen, J., Ellis, B. A., Peder-sen, P. K., Cooney, G. J., and Jensen, J. (2002). Acyl-CoA binding protein expression is fibre type specific and elevated in muscles from obese insulin-resistant Zucker rat. Diabetes 51, 449-454.
41. Frayn, K. N. (1983). Calculation of substrate oxidation rates in vivo from gaseous exchange. J. Appl. Physiol. 55, 628-634.
42. Frosig, C., Rose, A. J., Treebak, J. T., Kiens, B., Richter, E. A., and Wojtaszewski, J. F. (2007). Effects of endurance exercise training on insulin signaling in human skeletal muscle: interactions at the level of phosphatidylinositol 3-kinase, Akt, and AS160. Diabetes 56, 2093-2102.
43. Gibala, M. J., Little, J. P., van, E. M., Wilkin, G. P., Burgomaster, K. A., Safdar, A., Raha, S., and Tarnopolsky, M. A. (2006). Short-term sprint interval versus traditional endurance training: similar initial adaptations in human skeletal muscle and exercise performance. J. Physiol. (Lond.) 575, 901-911.
44. Gjedsted, J., Buhl, M., Nielsen, S., Schmitz, O., Vestergaard, E. T., Tonnesen, E., and Moller, N. (2011). Effects of adrenaline on lactate, glucose, lipid and protein metabolism in the placebo controlled bilaterally perfused human leg. Acta Physiol. (Oxf.) 202, 641-648.
45. Greiwe, J. S., Hickner, R. C., Hansen, P. A., Racette, S. B., Chen, M. M., and Holloszy, J. O. (1999). Effects of endurance exercise training on muscle glycogen accumulation in humans. J. Appl. Physiol. 87, 222-226.
46. Haemmerle, G., Lass, A., Zimmermann, R., Gorkiewicz, G., Meyer, C., Rozman, J., Heldmaier, G., Maier, R., Theussl, C., Eder, S., Kratky, D., Wagner, E. F., Klingenspor, M., Hoefler, G., and Zechner, R. (2006). Defective lipolysis and altered energy metabolism in mice lacking adipose triglyceride lipase. Science 312, 734-737.
47. Hawley, J. A., Schabort, E. J., Noakes, T. D., and Dennis, S. C. (1997). Carbohydrate-loading and exercise performance. An update. Sports Med. 24, 73-81.
48. He, J., and Kelley, D. E. (2004). Muscle glycogen content in type 2 diabetes mellitus. Am. J. Physiol. Endocrinol. Metab. 287, E1002-E1007.
49. Heath, G. W., Gavin, J. R. III, Hinderliter, J. M., Hagberg, J. M., Bloomfield, S. A., and Holloszy, J. O. (1983). Effects of exercise and lack of exercise on glucose tolerance and insulin sensitivity. J. Appl. Physiol. 55, 512-517.
50. Hermansen, L., Hultman, E., and Saltin, B. (1967). Muscle glycogen during prolonged severe exercise. Acta Physiol. Scand. 71, 129-139.
51. Hespel, P., and Richter, E. A. (1990). Glucose uptake and transport in contracting, perfused rat muscle with different pre-contraction glycogen concentrations. J. Physiol. (Lond.) 427, 347-359.
52. Hickner, R. C., Fisher, J. S., Hansen, P. A., Racette, S. B., Mier, C. M., Turner, M. J., and Holloszy, J. O. (1997). Muscle glycogen accumulation after endurance exercise in trained and untrained individuals. J. Appl. Physiol. 83, 897-903.
53. Hoehn, K. L., Salmon, A. B., Hohnen-Behrens, C., Turner, N., Hoy, A. J., Maghzal, G. J., Stocker, R., Van, R. H., Kraegen, E. W., Cooney, G. J., Richardson, A. R., and James, D. E. (2009). Insulin resistance is a cellular antioxidant defense mechanism. Proc. Natl. Acad. Sci. U.S.A. 106, 17787-17792.
54. Højlund, K., and Beck-Nielsen, H. (2006). Impaired glycogen synthase activity and mitochondrial dysfunction in skeletal muscle: markers or mediators of insulin resistance in type 2 diabetes? Curr. Diabetes Rev. 2, 375-395.
55. Houmard, J. A., Shaw, C. D., Hickey, M. S., and Tanner, C. J. (1999). Effect of short-term exercise training on insulin-stimulated PI 3-kinase activity in human skeletal muscle. Am. J. Physiol. 277, E1055-E1060.
56. Houmard, J. A., Shinebarger, M. H., Dolan, P. L., Leggettfrazier, N., Bruner, R. K., Mccammon, M. R., Israel, R. G., and Dohm, G. L. (1993). Exercise training increases GLUT-4 protein concentration in previously sedentary middle-aged men. Am. J. Physiol. 264, E896-E901.
57. Hoy, A. J., Bruce, C. R., Cederberg, A., Turner, N., James, D. E., Cooney, G. J., and Kraegen, E. W. (2007). Glucose infusion causes insulin resistance in skeletal muscle of rats without changes in Akt and AS160 phosphorylation. Am. J. Physiol. Endocrinol. Metab. 33, 1358-1364.
58. Hue, L., and Taegtmeyer,H. (2009). The Randle cycle revisited: a new head for an old hat.Am. J. Physiol. Endocrinol. Metab. 297, E578-E591.
59. Hunter, R. W., Treebak, J. T., Wojtaszewski, J. F., and Sakamoto, K. (2011). Molecular mechanism by which AMP-activated protein kinase activation promotes glycogen accumulation in muscle. Diabetes 60, 766-774.
60. Ivy, J. L. (1991). Muscle glycogen synthesis before and after exercise. Sports Med. 11, 6-19.
61. Ivy, J. L. (2001). Dietary strategies to promote glycogen synthesis after exercise. Can. J. Appl. Physiol. 26(Suppl.), S236-S245.
62. Ivy, J. L., Katz, A. L., Cutler, C. L., Sherman, W. M., and Coyle, E. F. (1988). Muscle glycogen synthesis after exercise: effect of time of carbohydrate ingestion. J. Appl. Physiol. 64, 1480-1485.
63. Jacobs,I.,Bar-Or, O.,Karlsson,J., Dotan, R., Tesch, P., Kaiser, P., and Inbar, O. (1982). Changes in muscle metabolites in females with 30-s exhaustive exercise. Med. Sci. Sports Exerc. 14, 457-460.
64. Jensen, J. (2009). "The role of skeletal muscle glycolysis in whole body metabolic regulation and type 2 diabetes," in Glycolysis: Regulation, Processes and Diseases, ed. H. Lithaw (New York: Nova Science Publishers, Inc.), 65-83.
65. Jensen,J.,Aslesen,R.,Ivy, J. L.,and Brørs, O. (1997). Role of glycogen concentration and epinephrine on glucose uptake in rat epitrochlearis muscle. Am. J. Physiol. 272, E649-E655.
66. Jensen, J., Brennesvik, E. O., Lai, Y. C., and Shepherd, P. R. (2007). GSK-3 regulation in skeletal muscles by adrenaline and insulin: evidence that PKA and PKB regulate different pools of GSK-3. Cell. Signal. 19, 204-210.
67. Jensen, J., Brørs, O., and Dahl, H. A. (1995). Different β-adrenergic receptor density in different rat skeletal muscle fibre types. Pharmacol. Toxicol. 76, 380-385.
68. Jensen, J., and Dahl, H. A. (1995). Adrenaline stimulated glycogen breakdown in rat epitrochlearis muscles: fibre type specificity and relation to phosphorylase transformation. Biochem. Mol. Biol. Int. 35, 145-154.
69. Jensen, J., Dahl, H. A., and Opstad, P. K. (1989). Adrenaline-mediated glycogenolysis in different skeletal muscle fibre types in the anaesthetized rat. Acta Physiol. Scand. 136, 229-233.
70. Jensen, J., Grønning-Wang, L. M., Jebens, E., Whitehead, J. P., Zorec, R., and Shepherd, P. R. (2008). Adrenaline potentiates insulin-stimulated PKB activation in the rat fast-twitch epitrochlearis muscle without affecting IRS-1 associated PI 3-kinase activity. Pflugers Arch. 456, 969-978.
71. Jensen, J., Jebens, E., Brennesvik, E. O., Ruzzin, J., Soos, M. A., Engebretsen, E. M., O'Rahilly, S., and White-head, J. P. (2006). Muscle glycogen inharmoniously regulates glycogen synthase activity,glucose uptake, and proximal insulin signaling. Am. J. Physiol. Endocrinol. Metab. 290, E154-E162.
72. Jensen, J., and Lai, Y. C. (2009). Regulation of muscle glycogen synthase phosphorylation and kinetic properties by insulin, exercise, adrenaline and role in insulin resistance. Arch. Physiol. Biochem. 115, 13-21.
73. Jensen, J., Ruge, T., Lai, Y. C., Svensson, M. K., and Eriksson, J. W. (2011). Effects of adrenaline on whole-body glucose metabolism and insulin-mediated regulation of glycogen synthase and PKB phosphorylation in human skeletal muscle. Metabolism 60, 215-226.
74. Jensen, J., Ruzzin, J., Jebens, E., Brennesvik, E. O., and Knardahl, S. (2005). Improved insulin-stimulated glucose uptake and glycogen synthase activation in rat skeletal muscles after adrenaline infusion: role of glycogen content and PKB phosphorylation. Acta Physiol. Scand. 184, 121-130.
75. Jessen, N., Pold, R., Buhl, E. S., Jensen, L. S., Schmitz, O., and Lund, S. (2003). Effects of AICAR and exercise on insulin-stimulated glucose uptake, signaling, and GLUT-4 content in rat muscles. J. Appl. Physiol. 94, 1373-1379.
76. Kawanaka,K., Han, D. H., Nolte, L. A., Hansen, P. A., Nakatani, A., and Holloszy, J. O. (1999). Decreased insulin-stimulated GLUT-4 translocation in glycogen-supercompensated muscles of exercised rats. Am. J. Physiol. 276, E907-E912.
77. Kawanaka, K., Nolte, L. A., Han, D. H., Hansen, P. A., and Holloszy, J. O. (2000). Mechanisms underlying impaired GLUT-4 translocation in glycogen-supercompensated muscles of exercised rats. Am. J. Physiol. Endocrinol. Metab. 279, E1311-E1318.
78. Kelley, D., Mitrakou, A., Marsh, H., Schwenk, F., Benn, J., Sonnenberg, G., Arcangeli, M., Aoki, T., Sorensen, J., and Berger, M. (1988). Skeletal muscle glycolysis, oxidation, and storage of an oral glucose load. J. Clin. Invest. 81, 1563-1571.
79. Kelley, D. E., and Mandarino, L. J. (1990). Hyperglycemia normalizes insulin-stimulated skeletal muscle glucose oxidation and storage in noninsulin-dependent diabetes mellitus. J. Clin. Invest. 86, 1999-2007.
80. Kim, Y. B., Nikoulina, S. E., Ciaraldi, T. P., Henry, R. R., and Kahn, B. B. (2000). Normal insulin-dependent activation of Akt/protein kinase B, with diminished activation of phos-phoinositide 3-kinase, in muscle in type 2 diabetes. J. Clin. Invest. 104, 733-741.
81. Knowler, W., Barret-Connor, E., Fowler, S., Hamman, R., Lachin, J. M., Walker, E., and Nathan, D. (2002). Reduction in the incidence of type 2 diabetes with lifestyle intervention or metformin. N. Engl. J. Med. 346, 393-403.
82. Koivisto, V. A., Yki-Järvinen, H., and Defronzo, R. A. (1986). Physical training and insulin sensitivity. Diabetes Metab. Rev. 1, 445-481.
83. Kollberg, G., Tulinius, M., Gilljam, T., Ostman-Smith, I., Forsander, G., Jotorp, P., Oldfors, A., and Holme, E. (2007). Cardiomyopathy and exercise intolerance in muscle glycogen storage disease 0. N. Engl. J. Med. 357, 1507-1514.
84. Lai, Y. C., Lin, F. C., and Jensen, J. (2009). Glycogen content regulates insulin-but not contraction-mediated glycogen synthase activation in the rat slow-twitch soleus muscles. Acta Physiol. (Oxf.) 197, 139-150.
85. Lai, Y. C., Stuenaes, J. T., Kuo, C. H., and Jensen, J. (2010a). Insulin-stimulated glycogen synthesis and glycogen synthase activation after electrical stimulation of epitrochlearis muscles with different initial glycogen contents. Arch. Physiol. Biochem. 116, 116-127.
86. Lai, Y. C., Zarrinpashneh, E., and Jensen, J. (2010b). Additive effect of contraction and insulin on glucose uptake and glycogen synthase in muscle with different glyco-gen contents. J. Appl. Physiol. 108, 1106-1115.
87. Lai, Y. C., Stuenæs, J. T., Kuo, C. H., and Jensen, J. (2007). Glycogen content and contraction regulate glycogen synthase phosphorylation and affinity for UDP-glucose in rat skeletal muscles. Am. J. Physiol. Endocrinol. Metab. 293, E1622-E1629.
88. Larance, M., Ramm, G., and James, D. E. (2008). The GLUT4 code. Mol. Endocrinol. 22, 226-233.
89. Laurent, D., Petersen, K. F., Russell, R. R., Cline, G. W., and Shulman, G. I. (1998). Effect of epinephrine on muscle glycogenolysis and insulin-stimulated muscle glycogen synthesis in humans. Am. J. Physiol. 274, E130-E138.
90. Lauritzen, H. P., Ploug, T., Ai, H., Donsmark, M., Prats, C., and Galbo, H. (2008). Denervation and high-fat diet reduce insulin signaling in T-tubules in skeletal muscle of living mice. Diabetes 57, 13-23.
91. Maarbjerg, S. J., Sylow, L., and Richter, E. A. (2011). Current understanding of increased insulin sensitivity after exercise-emerging candidates. Acta Physiol. (Oxf.) 202, 323-335.
92. Madsen, K., Pedersen, P. K., Rose, P., and Richter, E. A. (1990). Carbohydrate supercompensation and muscle glycogen utilization during exhaustive running in highly trained athletes. Eur. J. Appl. Physiol. 61, 467-472.
93. Magnusson, I., Rothman, D. L., Katz, L. D., Shulman,R. G., and Shulman, G. I. (1992). Increased rateof gluconeo-genesis in type II diabetes mellitus. A 13C nuclear magnetic resonance study. J. Clin. Invest. 90, 1323-1327.
94. McManus, E. J., Sakamoto, K., Armit, L. J., Ronaldson, L., Shpiro, N., Marquez, R., and Alessi, D. R. (2005). Role that phosphorylation of GSK3 plays in insulin and Wnt signalling defined by knockin analysis. EMBO J. 24, 1571-1583.
95. Meléndez, R., Meléndez-Hevia, E., and Canela, E. I. (1999). The fractal structure of glycogen: a clever solution to optimize cell metabolism. Biophys. J. 77, 1327-1332.
96. Mevorach, M., Giacca, A., Aharon, Y., Hawkins, M., Shamoon, H., and Rossetti, L. (1998). Regulation of endogenous glucose production by glucose per se is impaired in type 2 diabetes mellitus. J. Clin. Invest. 102, 744-753.
97. Mikines, K. J., Sonne, B., Farrell, P. A., Tronier, B., and Galbo, H. (1988). Effect of physical exercise on sensitivity and responsiveness to insulin in humans. Am. J. Physiol. 254, E248-E259.
98. Mikines, K. J., Sonne, B., Farrell, P. A., Tronier, B., and Galbo, H. (1989). Effect of training on the dose-response relationship for insulin action in men. J. Appl. Physiol. 66, 695-703.
99. Morino, K., Petersen, K. F., Dufour, S., Befroy, D., Frattini, J., Shatzkes, N., Neschen, S., White, M. F., Bilz, S., Sono, S., Pypaert, M., and Shulman, G. I. (2005). Reduced mitochondrial density and increased IRS-1 ser-ine phosphorylation in muscle of insulin-resistant offspring of type 2 diabetic parents. J. Clin. Invest. 115, 3587-3593.
100. Musi, N., Hayashi, T., Fujii, N., Hirshman, M. F., Witters, L. A., and Goodyear, L. J. (2001). AMP-activated protein kinase activity and glucose uptake in rat skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 280, E677-E684.
101. Nieman, D. C., Carlson, K. A., Brandstater, M. E., Naegele, R. T., and Blankenship, J. W. (1987). Running endurance in 27-h-fasted humans. J. Appl. Physiol. 63, 2502-2509.
102. Nolte, L. A., Gulve, E. A., and Holloszy, J. O. (1994). Epinephrine-induced in vivo muscle glycogen depletion enhances insulin sensitivity of glucose transport. J. Appl. Physiol. 76, 2054-2058.
103. Ortenblad, N., Nielsen, J., Saltin, B., and Holmberg, H. C. (2011). Role of glycogen availability in sarcoplasmic reticulum Ca2+ kinetics in human skeletal muscle. J. Physiol. (Lond.) 589, 711-725.
104. Pederson, B. A., Schroeder, J. M., Parker, G. E., Smith, M. W., Paoli-Roach, A. A., and Roach, P. J. (2005). Glucose metabolism in mice lacking muscle glycogen synthase. Diabetes 54, 3466-3473.
105. Peronnet, F., and Massicotte, D. (1991). Table of nonprotein respiratory quotient: an update. Can. J. Sport Sci. 16, 23-29.
106. Petersen, K. F., Dufour, S., Savage, D. B., Bilz, S., Solomon, G., Yonemitsu, S., Cline, G. W., Befroy, D., Zemany, L., Kahn, B. B., Papademetris, X., Rothman, D. L., and Shulman, G. I. (2007). The role of skeletal muscle insulin resistance in the pathogenesis of the metabolic syndrome. Proc. Natl. Acad. Sci. U.S.A. 104, 12587-12594.
107. Prebil, M., Jensen, J., Zorec, R., and Kreft, M. (2011). Astrocytes and energy metabolism. Arch. Physiol. Biochem. 117, 64-69.
108. Qvisth, V., Hagstrom-Toft, E., Moberg, E., Sjoberg, S., and Bolinder, J. (2007). Lactate release from adipose tissue and skeletal muscle in vivo: defective insulin regulation in insulin-resistant obese women. Am. J. Physiol. Endocrinol. Metab. 292, E709-E714.
109. Richards, J. C., Johnson, T. K., Kuzma, J. N., Lonac, M. C., Schweder, M. M., Voyles, W. F., and Bell, C. (2010). Short-term sprint interval training increases insulin sensitivity in healthy adults but does not affect the thermogenic response to beta-adrenergic stimulation. J. Physiol. (Lond.) 588, 2961-2972.
110. Richter, E. A., Hansen, S. A., and Hansen, B. F. (1988). Mechanisms limiting glycogen storage in muscle during prolonged insulin stimulation. Am. J. Physiol. 255, E621-E628.
111. Romijn, J. A., Coyle, E. F., Sidossis, L. S., Gastaldelli, A., Horowitz, J. F., Endert, E., and Wolfe, R. R. (1993). Regulation of endogenous fat and carbohydrate metabolism in relation to exercise intensity and duration. Am. J. Physiol. 265, E380-E391.
112. Ruzzin, J., Wagman, A. S., and Jensen, J. (2005). Glucocorticoids-induced insulin resistance: defects in insulin signalling and the effects of a selective glycogen synthase kinase-3 inhibitor. Diabetologia 48, 2119-2130.
113. Sakamoto, K., and Holman, G. D. (2008). Emerging role for AS160/TBC1D4 and TBC1D1 in the regulation of GLUT4 traffic. Am. J. Physiol. Endocrinol. Metab. 295, E29-E37.
114. Saltin, B., and Karlsson, J. (1971). "Muscle glycogen utilization during work of different work intensities," in Muscle Metabolism During Exercise (Stockholm: Karolinska Institute), 289-299.
115. Samuel, V. T., Petersen, K. F., and Shulman, G. I. (2010). Lipid-induced insulin resistance: unravelling the mechanism. Lancet 375, 2267-2277.
116. Sarbassov, D. D., Guertin, D. A., Ali, S. M., and Sabatini, D. M. (2005). Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 307, 1098-1101.
117. Schultze, S. M., Jensen, J., Hemmings, B. A., Tschopp, O., and Niessen, M. (2011). Promiscuous affairs of PKB/AKT isoforms in metabolism. Arch. Physiol. Biochem. 117, 70-77.
118. Shepherd, P. R. (2005). Mechanisms regulating phosphoinositide 3-kinase signalling in insulin-sensitive tissues. Acta Physiol. Scand. 183, 3-12.
119. Shulman, G. I., Rothman, D. L., Jue, T., Stein, P., Defronzo, R. A., and Shulman, R. G. (1990). Quantification of muscle glycogen synthesis in normal subjects and subjects with non-insulin-dependent diabetes by 13C nuclear magnetic resonance spectroscopy. N. Engl. J. Med. 322, 223-228.
120. Simonsen, L., Bulow, J., Madsen, J., and Christensen, N. J. (1992). Thermogenic response to epinephrine in the forearm and abdominal subcutaneous adipose tissue. Am. J. Physiol. 263, E850-E855.
121. Taniguchi, C. M., Emanuelli, B., and Kahn, C. R. (2006). Critical nodes in signalling pathways: insights into insulin action. Nat. Rev. Mol. Cell Biol. 7, 85-96.
122. Taylor, R., Magnusson, I., Rothman, D. L., Cline, G. W., Caumo, A., Cobelli, C., and Shulman, G. I. (1996). Direct assessment of liver glycogen storage by 13C nuclear magnetic resonance spectroscopy and regulation of glucose homeostasis after a mixed meal in normal subjects. J. Clin. Invest. 97, 126-132.
123. Taylor, R., Price, T. B., Katz, L. D., Shulman, R. G., and Shulman, G. I. (1993). Direct measurement of change in muscle glycogen concentration after a mixed meal in normal subjects. Am. J. Physiol. 265, E224-E229.
124. Vaag, A., Damsbo, P., Hother-Nielsen, O., and Beck-Nielsen, H. (1992). Hyperglycaemia compensates for the defects in insulin-mediated glucose metabolism and in the activation of glycogen synthase in the skeletal muscle of patients with type 2 (non-insulin-dependent) diabetes mellitus. Diabetologia 35, 80-88.
125. van Loon, L. J., Greenhaff, P. L., Constantin-Teodosiu, D., Saris, W. H., and Wagenmakers, A. J. (2001). The effects of increasing exercise intensity on muscle fuel utilisation in humans. J. Physiol. (Lond.) 536, 295-304.
126. Vendelbo, M. H., Clasen, B. F., Treebak, J. T., Moller, L., Krusenstjerna-Hafstrom, T., Madsen, M., Nielsen, T. S., Stodkilde-Jorgensen, H., Pedersen, S. B., Jorgensen, J. O., Goodyear, L. J., Wojtaszewski, J. F., Moller, N., and Jessen, N. (2011). Insulin resistance after a 72 hour fast is associated with impaired AS160 phosphorylation and accumulation of lipid and glycogen in human skeletal muscle. Am. J. Physiol. Endocrinol. Metab. PMID: 22028408. [Epub ahead of print].
127. Vind, B. F., Pehmoller, C., Tree-bak, J. T., Birk, J. B., Hey-Mogensen, M., Beck-Nielsen, H., Zierath, J. R., Wojtaszewski, J. F., and Hojlund, K. (2011). Impaired insulin-induced site-specific phosphorylation of TBC1 domain family, member 4 (TBC1D4) in skeletal muscle of type 2 diabetes patients is restored by endurance exercise-training. Diabetologia 54, 157-167.
128. Wadley, G. D., Konstantopoulos, N., Macaulay, L., Howlett, K. F., Garnham, A., Hargreaves, M., and Cameron-Smith, D. (2007). Increased insulin-stimulated Akt pSer473 and cytosolic SHP2 protein abundance in human skeletal muscle following acute exercise and short-term training. J. Appl. Physiol. 102, 1624-1631.
129. Wojtaszewski,J. F.,Higaki,Y., Hirshman, M. F., Michael, M. D., Dufresne, S. D., Kahn, C. R., and Goodyear, L. J. (1999). Exercise modulates postre-ceptor insulin signaling and glucose transport in muscle-specific insulin receptor knockout mice. J. Clin. Invest. 104, 1257-1264.
130. Wojtaszewski, J. F., Nielsen, J. N., and Richter, E. A. (2002). Invited review: effect of acute exercise on insulin signaling and action in humans. J. Appl. Physiol. 93, 384-392.
131. Young, J. C., Garthwaite, S. M., Bryan, J. E., Cartier, L.-J., and Holloszy, J. O. (1983). Carbohydrate feeding speeds reversal of enhanced glucose uptake in muscle after exercise. Am. J. Physiol. 245, R684-R688.