Mechanisms for greater insulin-stimulated glucose uptake in normal and insulin-resistant skeletal muscle after acute exercise

American Journal of Physiology - Endocrinology and Metabolism

Volumn 309, Issue 12, 2015, Pages E949-E959

  Cartee, Gregory D ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Akt substrate of 160 kDa; AMP activated protein kinase; Glucose transporter 4; Insulin sensitivity; Physical activity

Indexed keywords

GLUCOSE TRANSPORTER 4; INSULIN; INSULIN RECEPTOR; PROTEIN KINASE B; GLUCOSE;

ACTIN POLYMERIZATION; AUTOPHOSPHORYLATION; COMPARATIVE STUDY; CONTROLLED STUDY; ENDOCYTOSIS; ENZYME ACTIVITY; EX VIVO STUDY; EXERCISE; EXOCYTOSIS; GLUCOSE INFUSION; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; GLYCOGEN MUSCLE LEVEL; GLYCOGEN SYNTHESIS; HUMAN; INSULIN RESISTANCE; INSULIN SENSITIVITY; NUCLEAR MAGNETIC RESONANCE; PHYSICAL ACTIVITY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; ANIMAL; BIOLOGICAL MODEL; DRUG EFFECTS; METABOLISM; PHYSIOLOGY;

ANIMALS; EXERCISE; GLUCOSE; HUMANS; INSULIN; INSULIN RESISTANCE; MODELS, BIOLOGICAL; MUSCLE, SKELETAL; PHYSICAL EXERTION;

EID: 84959187675     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00416.2015     Document Type: Review

References (131)

1. Arias EB, Kim J, Funai K, Cartee GD. Prior exercise increases phosphorylation of Akt substrate of 160 kDa (AS160) in rat skeletal muscle. Am J Physiol Endocrinol Metab 292: E1191-E1200, 2007.
2. Betts JJ, Sherman WM, Reed MJ, Gao JP. Duration of improved muscle glucose uptake after acute exercise in obese Zucker rats. Obes Res 1: 295-302, 1993.
3. Blair DR, Funai K, Schweitzer GG, Cartee GD. A myosin II ATPase inhibitor reduces force production, glucose transport, and phosphorylation of AMPK and TBC1D1 in electrically stimulated rat skeletal muscle. Am J Physiol Endocrinol Metab 296: E993-E1002, 2009.
4. Bogardus C, Thuillez P, Ravussin E, Vasquez B, Narimiga M, Azhar S. Effect of muscle glycogen depletion on in vivo insulin action in man. J Clin Invest 72: 1605-1610, 1983.
5. Bonen A, Tan MH, Watson-Wright WM. Effects of exercise on insulin binding and glucose metabolism in muscle. Can J Physiol Pharmacol 62: 1500-1504, 1984.
6. Boucher J, Kleinridders A, Kahn CR. Insulin receptor signaling in normal and insulin-resistant states. Cold Spring Harbor Perspect Biol 6: pii: a009191, 2014.
7. Bouzakri K, Zachrisson A, Al-Khalili L, Zhang BB, Koistinen HA, Krook A, Zierath JR. siRNA-based gene silencing reveals specialized roles of IRS-1/Akt2 and IRS-2/Akt1 in glucose and lipid metabolism in human skeletal muscle. Cell Metab 4: 89-96, 2006.
8. Brewer PD, Habtemichael EN, Romenskaia I, Mastick CC, Coster AC. Insulin-regulated Glut4 translocation: membrane protein trafficking with six distinctive steps. J Biol Chem 289: 17280-17298, 2014.
9. Burstein R, Galun E. Exercise-induced hyponatremia-as rare as believed? Med Sci Sports Exerc 22: 879, 1990.
10. Cartee GD. Roles of TBC1D1 and TBC1D4 in insulin-and exercisestimulated glucose transport of skeletal muscle. Diabetologia 58: 19-30, 2015.
11. Cartee GD, Briggs-Tung C, Kietzke EW. Persistent effects of exercise on skeletal muscle glucose transport across the life-span of rats. J Appl Physiol 75: 972-978, 1993.
12. Cartee GD, Holloszy JO. Exercise increases susceptibility of muscle glucose transport to activation by various stimuli. Am J Physiol Endocrinol Metab 258: E390-E393, 1990.
13. Cartee GD, Young DA, Sleeper MD, Zierath J, Wallberg-Henriksson H, Holloszy JO. Prolonged increase in insulin-stimulated glucose transport in muscle after exercise. Am J Physiol Endocrinol Metab 256: E494-E499, 1989.
14. Castorena CM, Arias EB, Sharma N, Cartee GD. Postexercise improvement in insulin-stimulated glucose uptake occurs concomitant with greater AS160 phosphorylation in muscle from normal and insulinresistant rats. Diabetes 63: 2297-2308, 2014.
15. Castorena CM, Arias EB, Sharma N, Cartee GD. Effects of a brief high-fat diet and acute exercise on the mTORC1 and IKK/NF-kappaB pathways in rat skeletal muscle. Appl Physiol Nutr Metab 40: 251-262, 2015.
16. Chen Q, Quan C, Xie B, Chen L, Zhou S, Toth R, Campbell DG, Lu S, Shirakawa R, Horiuchi H, Li C, Yang Z, MacKintosh C, Wang HY, Chen S. GARNL1, a major RalGAP alpha subunit in skeletal muscle, regulates insulin-stimulated RalA activation and GLUT4 trafficking via interaction with 14-3-3 proteins. Cell Signal 26: 1636-1648, 2014.
17. Chen XW, Leto D, Xiong T, Yu G, Cheng A, Decker S, Saltiel AR. A Ral GAP complex links PI 3-kinase/Akt signaling to RalA activation in insulin action. Mol Biol Cell 22: 141-152, 2011.
18. Chiu TT, Jensen TE, Sylow L, Richter EA, Klip A. Rac1 signalling towards GLUT4/glucose uptake in skeletal muscle. Cell Signal 23: 1546-1554, 2011.
19. Constable SH, Favier RJ, Cartee GD, Young DA, Holloszy JO. Muscle glucose transport: interactions of in vitro contractions, insulin, and exercise. J Appl Physiol 64: 2329-2332, 1988.
20. DeFronzo RA. Lilly lecture 1987. The triumvirate: beta-cell, muscle, liver. A collusion responsible for NIDDM. Diabetes 37: 667-687, 1988.
21. DeFronzo RA, Jacot E, Jequier E, Maeder E, Wahren J, Felber JP. The effect of insulin on the disposal of intravenous glucose. Results from indirect calorimetry and hepatic and femoral venous catheterization. Diabetes 30: 1000-1007, 1981.
22. Derave W, Hansen BF, Lund S, Kristiansen S, Richter EA. Muscle glycogen content affects insulin-stimulated glucose transport and protein kinase B activity. Am J Physiol Endocrinol Metab 279: E947-E955, 2000.
23. Devlin JT, Hirshman M, Horton ED, Horton ES. Enhanced peripheral and splanchnic insulin sensitivity in NIDDM men after single bout of exercise. Diabetes 36: 434-439, 1987.
24. Devlin JT, Horton ES. Effects of prior high-intensity exercise on glucose metabolism in normal and insulin-resistant men. Diabetes 34: 973-979, 1985.
25. Douen AG, Ramlal T, Rastogi S, Bilan PJ, Cartee GD, Vranic M, Holloszy JO, Klip A. Exercise induces recruitment of the "insulinresponsive glucose transporter". Evidence for distinct intracellular insulin-and exercise-recruitable transporter pools in skeletal muscle. J Biol Chem 265: 13427-13430, 1990.
26. Dumke CL, Kim J, Arias EB, Cartee GD. Role of kallikrein-kininogen system in insulin-stimulated glucose transport after muscle contractions. J Appl Physiol 92: 657-664, 2002.
27. Facchini FS, Hua N, Abbasi F, Reaven GM. Insulin resistance as a predictor of age-related diseases. J Clin Endocrinol Metab 86: 3574-3578, 2001.
28. Farese RV, Sajan MP. Metabolic functions of atypical protein kinase C: "good" and "bad" as defined by nutritional status. Am J Physiol Endocrinol Metab 298: E385-E394, 2010.
29. Farese RV, Sajan MP, Yang H, Li P, Mastorides S, Gower WR Jr, Nimal S, Choi CS, Kim S, Shulman GI, Kahn CR, Braun U, Leitges M. Muscle-specific knockout of PKC-lambda impairs glucose transport and induces metabolic and diabetic syndromes. J Clin Invest 117: 2289-2301, 2007.
30. Fazakerley DJ, Holman GD, Marley A, James DE, Stockli J, Coster AC. Kinetic evidence for unique regulation of GLUT4 trafficking by insulin and AMP-activated protein kinase activators in L6 myotubes. J Biol Chem 285: 1653-1660, 2010.
31. Fisher JS, Gao J, Han DH, Holloszy JO, Nolte LA. Activation of AMP kinase enhances sensitivity of muscle glucose transport to insulin. Am J Physiol Endocrinol Metab 282: E18-E23, 2002.
32. Foley K, Boguslavsky S, Klip A. Endocytosis, recycling, and regulated exocytosis of glucose transporter 4. Biochemistry 50: 3048-3061, 2011.
33. Frosig C, Richter EA. Improved insulin sensitivity after exercise: focus on insulin signaling. Obesity (Silver Spring) 17, Suppl 3: S15-S20, 2009.
34. Frosig C, Roepstorff C, Brandt N, Maarbjerg SJ, Birk JB, Wojtaszewski JF, Richter EA, Kiens B. Reduced malonyl-CoA content in recovery from exercise correlates with improved insulin-stimulated glucose uptake in human skeletal muscle. Am J Physiol Endocrinol Metab 296: E787-E795, 2009.
35. Frøsig C, Sajan MP, Maarbjerg SJ, Brandt N, Roepstorff C, Wojtaszewski JF, Kiens B, Farese RV, Richter EA. Exercise improves phosphatidylinositol-3,4,5-trisphosphate responsiveness of atypical protein kinase C and interacts with insulin signalling to peptide elongation in human skeletal muscle. J Physiol 582: 1289-1301, 2007.
36. Fueger PT, Shearer J, Bracy DP, Posey KA, Pencek RR, McGuinness OP, Wasserman DH. Control of muscle glucose uptake: test of the rate-limiting step paradigm in conscious, unrestrained mice. J Physiol 562: 925-935, 2005.
37. Funai K, Schweitzer GG, Castorena CM, Kanzaki M, Cartee GD. In vivo exercise followed by in vitro contraction additively elevates subsequent insulin-stimulated glucose transport by rat skeletal muscle. Am J Physiol Endocrinol Metab 298: E999-E1010, 2010.
38. Funai K, Schweitzer GG, Sharma N, Kanzaki M, Cartee GD. Increased AS160 phosphorylation, but not TBC1D1 phosphorylation, with increased postexercise insulin sensitivity in rat skeletal muscle. Am J Physiol Endocrinol Metab 297: E242-E251, 2009.
39. Gao J, Gulve EA, Holloszy JO. Contraction-induced increase in muscle insulin sensitivity: requirement for a serum factor. Am J Physiol Endocrinol Metab 266: E186-E192, 1994.
40. Gao J, Sherman WM, McCune SA, Osei K. Effects of acute running exercise on whole body insulin action in obese male SHHF/Mcc-facp rats. J Appl Physiol 77: 534-541, 1994.
41. Geiger PC, Han DH, Wright DC, Holloszy JO. How muscle insulin sensitivity is regulated: testing of a hypothesis. Am J Physiol Endocrinol Metab 291: E1258-E1263, 2006.
42. Gonzalez E, McGraw TE. Insulin-modulated Akt subcellular localization determines Akt isoform-specific signaling. Proc Natl Acad Sci USA 106: 7004-7009, 2009.
43. Goodpaster BH, Bertoldo A, Ng JM, Azuma K, Pencek RR, Kelley C, Price JC, Cobelli C, Kelley DE. Interactions among glucose delivery, transport, and phosphorylation that underlie skeletal muscle insulin resistance in obesity and type 2 diabetes: studies with dynamic PET imaging. Diabetes 63: 1058-1068, 2014.
44. Gulve EA, Cartee GD, Zierath JR, Corpus VM, Holloszy JO. Reversal of enhanced muscle glucose transport after exercise: roles of insulin and glucose. Am J Physiol Endocrinol Metab 259: E685-E691, 1990.
45. Haffner SM. Epidemiology of insulin resistance and its relation to coronary artery disease. Am J Cardiol 84: 11J-14J, 1999.
46. Hamada T, Arias EB, Cartee GD. Increased submaximal insulinstimulated glucose uptake in mouse skeletal muscle after treadmill exercise. J Appl Physiol 101: 1368-1376, 2006.
47. Hansen PA, Nolte LA, Chen MM, Holloszy JO. Increased GLUT-4 translocation mediates enhanced insulin sensitivity of muscle glucose transport after exercise. J Appl Physiol 85: 1218-1222, 1998.
48. Hegarty BD, Furler SM, Ye J, Cooney GJ, Kraegen EW. The role of intramuscular lipid in insulin resistance. Acta Physiol Scand 178: 373-383, 2003.
49. Henriksen EJ. Invited review: Effects of acute exercise and exercise training on insulin resistance. J Appl Physiol 93: 788-796, 2002.
50. Høeg LD, Sjøberg KA, Jeppesen J, Jensen TE, Frøsig C, Birk JB, Bisiani B, Hiscock N, Pilegaard H, Wojtaszewski JF, Richter EA, Kiens B. Lipid-induced insulin resistance affects women less than men and is not accompanied by inflammation or impaired proximal insulin signaling. Diabetes 60: 64-73, 2011.
51. Hoffman NJ, Elmendorf JS. Signaling, cytoskeletal and membrane mechanisms regulating GLUT4 exocytosis. Trends Endocrinol Metab 22: 110-116, 2011.
52. Holloszy JO. Exercise-induced increase in muscle insulin sensitivity. J Appl Physiol 99: 338-343, 2005.
53. Huang S, Czech MP. The GLUT4 glucose transporter. Cell Metab 5: 237-252, 2007.
54. Irimia JM, Tagliabracci VS, Meyer CM, Segvich DM, DePaoli-Roach AA, Roach PJ. Muscle Glycogen Remodeling and Glycogen Phosphate Metabolism Following Exhaustive Exercise of Wild Type and Laforin Knockout Mice. J Biol Chem 290: 22686-22698, 2015.
55. Ishiki M, Klip A. Minireview: recent developments in the regulation of glucose transporter-4 traffic: new signals, locations, and partners. Endocrinology 146: 5071-5078, 2005.
56. Iwabe M, Kawamoto E, Koshinaka K, Kawanaka K. Increased postexercise insulin sensitivity is accompanied by increased AS160 phosphorylation in slow-twitch soleus muscle. Physiol Rep 2: pii: e12162, 2014.
57. JeBailey L, Wanono O, Niu W, Roessler J, Rudich A, Klip A. Ceramide-and oxidant-induced insulin resistance involve loss of insulindependent Rac-activation and actin remodeling in muscle cells. Diabetes 56: 394-403, 2007.
58. Jensen J, Rustad PI, Kolnes AJ, Lai YC. The role of skeletal muscle glycogen breakdown for regulation of insulin sensitivity by exercise. Front Physiol 2: 112, 2011.
59. Jensen TE, Richter EA. Regulation of glucose and glycogen metabolism during and after exercise. J Physiol 590: 1069-1076, 2012.
60. Jovanovic A, Leverton E, Solanky B, Ravikumar B, Snaar JE, Morris PG, Taylor R. The second-meal phenomenon is associated with enhanced muscle glycogen storage in humans. Clin Sci (Lond) 117: 119-127, 2009.
61. Karlsson HK, Ahlsen M, Zierath JR, Wallberg-Henriksson H, Koistinen HA. Insulin signaling and glucose transport in skeletal muscle from first-degree relatives of type 2 diabetic patients. Diabetes 55: 1283-1288, 2006.
62. Karlsson HK, Chibalin AV, Koistinen HA, Yang J, Koumanov F, Wallberg-Henriksson H, Zierath JR, Holman GD. Kinetics of GLUT4 trafficking in rat and human skeletal muscle. Diabetes 58: 847-854, 2009.
63. Kim J, Solis RS, Arias EB, Cartee GD. Postcontraction insulin sensitivity: relationship with contraction protocol, glycogen concentration, and 5= AMP-activated protein kinase phosphorylation. J Appl Physiol 96: 575-583, 2004.
64. Kjobsted R, Treebak JT, Fentz J, Lantier L, Viollet B, Birk JB, Schjerling P, Björnholm M, Zierath JR, Wojtaszewski JF. Prior AICAR stimulation increases insulin sensitivity in mouse skeletal muscle in an AMPK-dependent manner. Diabetes 64: 2042-2055, 2015.
65. Klip A, Sun Y, Chiu TT, Foley KP. Signal transduction meets vesicle traffic: the software and hardware of GLUT4 translocation. Am J Physiol Cell Physiol 306: C879-C886, 2014.
66. Kolnes AJ, Birk JB, Eilertsen E, Stuenaes JT, Wojtaszewski JF, Jensen J. Epinephrine-stimulated glycogen breakdown activates glycogen synthase and increases insulin-stimulated glucose uptake in epitrochlearis muscles. Am J Physiol Endocrinol Metab 308: E231-E240, 2015.
67. Koshinaka K, Sano A, Howlett KF, Yamazaki T, Sasaki M, Sakamoto K, Kawanaka K. Effect of high-intensity intermittent swimming on postexercise insulin sensitivity in rat epitrochlearis muscle. Metabolism 57: 749-756, 2008.
68. Krook A, Björnholm M, Galuska D, Jiang XJ, Fahlman R, Myers MG Jr, Wallberg-Henriksson H, Zierath JR. Characterization of signal transduction and glucose transport in skeletal muscle from type 2 diabetic patients. Diabetes 49: 284-292, 2000.
69. Kumari M, Brunner E, Fuhrer R. Minireview: mechanisms by which the metabolic syndrome and diabetes impair memory. J Gerontol A Biol Sci Med Sci 55: B228-B232, 2000.
70. Leto D, Saltiel AR. Regulation of glucose transport by insulin: traffic control of GLUT4. Nat Rev Mol Cell Biol 13: 383-396, 2012.
71. Leto D, Uhm M, Williams A, Chen XW, Saltiel AR. Negative regulation of the RalGAP complex by 14-3-3. J Biol Chem 288: 9272-9283, 2013.
72. Levinger I, Jerums G, Stepto NK, Parker L, Serpiello FR, McConell GK, Anderson M, Hare DL, Byrnes E, Ebeling PR, Seeman E. The effect of acute exercise on undercarboxylated osteocalcin and insulin sensitivity in obese men. J Bone Miner Res 29: 2571-2576, 2014.
73. Lucidi P, Rossetti P, Porcellati F, Pampanelli S, Candeloro P, Andreoli AM, Perriello G, Bolli GB, Fanelli CG. Mechanisms of insulin resistance after insulin-induced hypoglycemia in humans: the role of lipolysis. Diabetes 59: 1349-1357, 2010.
74. Maarbjerg SJ, Jørgensen SB, Rose AJ, Jeppesen J, Jensen TE, Treebak JT, Birk JB, Schjerling P, Wojtaszewski JF, Richter EA. Genetic impairment of AMPK_2 signaling does not reduce muscle glucose uptake during treadmill exercise in mice. Am J Physiol Endocrinol Metab 297: E924-E934, 2009.
75. Maarbjerg SJ, Sylow L, Richter EA. Current understanding of increased insulin sensitivity after exercise-emerging candidates. Acta Physiol (Oxf) 202: 323-335, 2011.
76. McBride A, Ghilagaber S, Nikolaev A, Hardie DG. The glycogenbinding domain on the AMPK beta subunit allows the kinase to act as a glycogen sensor. Cell Metab 9: 23-34, 2009.
77. McConell GK, Kaur G, Falcao-Tebas F, Hong YH, Gatford KL. Acute exercise increases insulin sensitivity in adult sheep: a new preclinical model. Am J Physiol Regul Integr Comp Physiol 308: R500-R506, 2015.
78. Miinea CP, Sano H, Kane S, Sano E, Fukuda M, Peranen J, Lane WS, Lienhard GE. AS160, the Akt substrate regulating GLUT4 translocation, has a functional Rab GTPase-activating protein domain. Biochem J 391: 87-93, 2005.
79. Mikines KJ, Sonne B, Farrell PA, Tronier B, Galbo H. Effect of physical exercise on sensitivity and responsiveness to insulin in humans. Am J Physiol Endocrinol Metab 254: E248-E259, 1988.
80. Musi N, Hayashi T, Fujii N, Hirshman MF, Witters LA, Goodyear LJ. AMP-activated protein kinase activity and glucose uptake in rat skeletal muscle. Am J Physiol Endocrinol Metab 280: E677-E684, 2001.
81. Nagasawa J, Sato Y, Ishiko T. Time course of in vivo insulin sensitivity after a single bout of exercise in rats. Int J Sports Med 12: 399-402, 1991.
82. Nolte LA, Gulve EA, Holloszy JO. Epinephrine-induced in vivo muscle glycogen depletion enhances insulin sensitivity of glucose transport. J Appl Physiol 76: 2054-2058, 1994.
83. Oakes ND, Bell KS, Furler SM, Camilleri S, Saha AK, Ruderman NB, Chisholm DJ, Kraegen EW. Diet-induced muscle insulin resistance in rats is ameliorated by acute dietary lipid withdrawal or a single bout of exercise: parallel relationship between insulin stimulation of glucose uptake and suppression of long-chain fatty acyl-CoA. Diabetes 46: 2022-2028, 1997.
84. Oliveira AG, Carvalho BM, Tobar N, Ropelle ER, Pauli JR, Bagarolli RA, Guadagnini D, Carvalheira JB, Saad MJ. Physical exercise reduces circulating lipopolysaccharide and TLR4 activation and improves insulin signaling in tissues of DIO rats. Diabetes 60: 784-796, 2011.
85. Pauli JR, Ropelle ER, Cintra DE, Carvalho-Filho MA, Moraes JC, De Souza CT, Velloso LA, Carvalheira JB, Saad MJ. Acute physical exercise reverses S-nitrosation of the insulin receptor, insulin receptor substrate 1 and protein kinase B/Akt in diet-induced obese Wistar rats. J Physiol 586: 659-671, 2008.
86. Pehmøller C, Brandt N, Birk JB, Høeg LD, Sjøberg KA, Goodyear LJ, Kiens B, Richter EA, Wojtaszewski JF. Exercise alleviates lipidinduced insulin resistance in human skeletal muscle-signaling interaction at the level of TBC1 domain family member 4. Diabetes 61: 2743-2752, 2012.
87. Pencek RR, James F, Lacy DB, Jabbour K, Williams PE, Fueger PT, Wasserman DH. Interaction of insulin and prior exercise in control of hepatic metabolism of a glucose load. Diabetes 52: 1897-1903, 2003.
88. Perseghin G, Price TB, Petersen KF, Roden M, Cline GW, Gerow K, Rothman DL, Shulman GI. Increased glucose transport-phosphorylation and muscle glycogen synthesis after exercise training in insulinresistant subjects. N Engl J Med 335: 1357-1362, 1996.
89. Polekhina G, Gupta A, Michell BJ, van Denderen B, Murthy S, Feil SC, Jennings IG, Campbell DJ, Witters LA, Parker MW, Kemp BE, Stapleton D. AMPK beta subunit targets metabolic stress sensing to glycogen. Curr Biol 13: 867-871, 2003.
90. Rasmussen BB, Hancock CR, Winder WW. Postexercise recovery of skeletal muscle malonyl-CoA, acetyl-CoA carboxylase, and AMP-activated protein kinase. J Appl Physiol 85: 1629-1634, 1998.
91. Richter EA, Derave W, Wojtaszewski JF. Glucose, exercise and insulin: emerging concepts. J Physiol 535: 313-322, 2001.
92. Richter EA, Garetto LP, Goodman MN, Ruderman NB. Muscle glucose metabolism following exercise in the rat: increased sensitivity to insulin. J Clin Invest 69: 785-793, 1982.
93. Richter EA, Hargreaves M. Exercise, GLUT4, and skeletal muscle glucose uptake. Physiol Rev 93: 993-1017, 2013.
94. Richter EA, Mikines KJ, Galbo H, Kiens B. Effect of exercise on insulin action in human skeletal muscle. J Appl Physiol 66: 876-885, 1989.
95. Ropelle ER, Pauli JR, Prada PO, de Souza CT, Picardi PK, Faria MC, Cintra DE, Fernandes MF, Flores MB, Velloso LA, Saad MJ, Carvalheira JB. Reversal of diet-induced insulin resistance with a single bout of exercise in the rat: the role of PTP1B and IRS-1 serine phosphorylation. J Physiol 577: 997-1007, 2006.
96. Rowland AF, Fazakerley DJ, James DE. Mapping insulin/GLUT4 circuitry. Traffic 12: 672-681, 2011.
97. Samuel VT, Petersen KF, Shulman GI. Lipid-induced insulin resistance: unravelling the mechanism. Lancet 375: 2267-2277, 2010.
98. Sano H, Kane S, Sano E, Miinea CP, Asara JM, Lane WS, Garner CW, Lienhard GE. Insulin-stimulated phosphorylation of a Rab GTPase-activating protein regulates GLUT4 translocation. J Biol Chem 278: 14599-14602, 2003.
99. Schenk S, Horowitz JF. Acute exercise increases triglyceride synthesis in skeletal muscle and prevents fatty acid-induced insulin resistance. J Clin Invest 117: 1690-1698, 2007.
100. Schenk S, Saberi M, Olefsky JM. Insulin sensitivity: modulation by nutrients and inflammation. J Clin Invest 118: 2992-3002, 2008.
101. Schweitzer GG, Arias EB, Cartee GD. Sustained postexercise increases in AS160 Thr642 and Ser588 phosphorylation in skeletal muscle without sustained increases in kinase phosphorylation. J Appl Physiol 113: 1852-1861, 2012.
102. Schweitzer GG, Cartee GD. Postexercise skeletal muscle glucose transport is normal in kininogen-deficient rats. Med Sci Sports Exerc 43: 1148-1153, 2011.
103. Sharoff CG, Hagobian TA, Malin SK, Chipkin SR, Yu H, Hirshman MF, Goodyear LJ, Braun B. Combining short-term metformin treatment and one bout of exercise does not increase insulin action in insulin-resistant individuals. Am J Physiol Endocrinol Metab 298: E815-E823, 2010.
104. Shoelson SE, Lee J, Goldfine AB. Inflammation and insulin resistance. J Clin Invest 116: 1793-1801, 2006.
105. Shoelson SE, Lee J, Yuan M. Inflammation and the IKK beta/I kappa B/NF-kappa B axis in obesity-and diet-induced insulin resistance. Int J Obes Relat Metab Disord 27, Suppl 3: S49-S52, 2003.
106. Steinberg GR, Kemp BE. AMPK in Health and Disease. Physiol Rev 89: 1025-1078, 2009.
107. Stöckli J, Fazakerley DJ, Coster AC, Holman GD, James DE. Muscling in on GLUT4 kinetics. Commun Integr Biol 3: 260-262, 2010.
108. Stöckli J, Fazakerley DJ, James DE. GLUT4 exocytosis. J Cell Sci 124: 4147-4159, 2011.
109. Stretton C, Evans A, Hundal HS. Cellular depletion of atypical PKC_ is associated with enhanced insulin sensitivity and glucose uptake in L6 rat skeletal muscle cells. Am J Physiol Endocrinol Metab 299: E402-E412, 2010.
110. Sylow L, Jensen TE, Kleinert M, Hojlund K, Kiens B, Wojtaszewski J, Prats C, Schjerling P, Richter EA. Rac1 signaling is required for insulin-stimulated glucose uptake and is dysregulated in insulin-resistant murine and human skeletal muscle. Diabetes 62: 1865-1875, 2013.
111. Sylow L, Kleinert M, Pehmoller C, Prats C, Chiu TT, Klip A, Richter EA, Jensen TE. Akt and Rac1 signaling are jointly required for insulinstimulated glucose uptake in skeletal muscle and downregulated in insulin resistance. Cell Signal 26: 323-331, 2014.
112. Takenaka N, Sumi Y, Matsuda K, Fujita J, Hosooka T, Noguchi T, Aiba A, Satoh T. Role for RalA downstream of Rac1 in skeletal muscle insulin signalling. Biochem J 469: 445-454, 2015.
113. Tan SX, Ng Y, Burchfield JG, Ramm G, Lambright DG, Stöckli J, James DE. The Rab GTPase-activating protein TBC1D4/AS160 contains an atypical phosphotyrosine-binding domain that interacts with plasma membrane phospholipids to facilitate GLUT4 trafficking in adipocytes. Mol Cell Biol 32: 4946-4959, 2012.
114. Tanaka S, Hayashi T, Toyoda T, Hamada T, Shimizu Y, Hirata M, Ebihara K, Masuzaki H, Hosoda K, Fushiki T, Nakao K. High-fat diet impairs the effects of a single bout of endurance exercise on glucose transport and insulin sensitivity in rat skeletal muscle. Metabolism 56: 1719-1728, 2007.
115. Thirone AC, Huang C, Klip A. Tissue-specific roles of IRS proteins in insulin signaling and glucose transport. Trends Endocrinol Metab 17: 72-78, 2006.
116. Thong FS, Derave W, Kiens B, Graham TE, Urso B, Wojtaszewski JF, Hansen BF, Richter EA. Caffeine-induced impairment of insulin action but not insulin signaling in human skeletal muscle is reduced by exercise. Diabetes 51: 583-590, 2002.
117. Toyoda T, Hayashi T, Miyamoto L, Yonemitsu S, Nakano M, Tanaka S, Ebihara K, Masuzaki H, Hosoda K, Inoue G, Otaka A, Sato K, Fushiki T, Nakao K. Possible involvement of the _1 isoform of 5=AMP-activated protein kinase in oxidative stress-stimulated glucose transport in skeletal muscle. Am J Physiol Endocrinol Metab 287: E166-E173, 2004.
118. Treebak JT, Frosig C, Pehmoller C, Chen S, Maarbjerg SJ, Brandt N, MacKintosh C, Zierath JR, Hardie DG, Kiens B, Richter EA, Pilegaard H, Wojtaszewski JF. Potential role of TBC1D4 in enhanced post-exercise insulin action in human skeletal muscle. Diabetologia 52: 891-900, 2009.
119. Treebak JT, Pehmoller C, Kristensen JM, Kjobsted R, Birk JB, Schjerling P, Richter EA, Goodyear LJ, Wojtaszewski JF. Acute exercise and physiological insulin induce distinct phosphorylation signatures on TBC1D1 and TBC1D4 proteins in human skeletal muscle. J Physiol 592: 351-375, 2014.
120. Turban S, Hajduch E. Protein kinase C isoforms: mediators of reactive lipid metabolites in the development of insulin resistance. FEBS Lett 585: 269-274, 2011.
121. Ueda S, Kitazawa S, Ishida K, Nishikawa Y, Matsui M, Matsumoto H, Aoki T, Nozaki S, Takeda T, Tamori Y, Aiba A, Kahn CR, Kataoka T, Satoh T. Crucial role of the small GTPase Rac1 in insulinstimulated translocation of glucose transporter 4 to the mouse skeletal muscle sarcolemma. FASEB J 24: 2254-2261, 2010.
122. Um SH, D'Alessio D, Thomas G. Nutrient overload, insulin resistance, and ribosomal protein S6 kinase 1, S6K1. Cell Metab 3: 393-402, 2006.
123. Vendelbo MH, Møller AB, Treebak JT, Gormsen LC, Goodyear LJ, Wojtaszewski JF, Jørgensen JO, Møller N, Jessen N. Sustained AS160 and TBC1D1 phosphorylations in human skeletal muscle 30 min after a single bout of exercise. J Appl Physiol 117: 289-296, 2014.
124. Wallberg-Henriksson H, Constable SH, Young DA, Holloszy JO. Glucose transport into rat skeletal muscle: interaction between exercise and insulin. J Appl Physiol 65: 909-913, 1988.
125. Wang X, Patterson BW, Smith GI, Kampelman J, Reeds DN, Sullivan SA, Mittendorfer B. A _60-min brisk walk increases insulinstimulated glucose disposal but has no effect on hepatic and adipose tissue insulin sensitivity in older women. J Appl Physiol 114: 1563-1568, 2013.
126. Wojtaszewski JF, Hansen BF, Gade, Kiens B, Markuns JF, Goodyear LJ, Richter EA. Insulin signaling and insulin sensitivity after exercise in human skeletal muscle. Diabetes 49: 325-331, 2000.
127. Wojtaszewski JF, Hansen BF, Kiens B, Richter EA. Insulin signaling in human skeletal muscle: time course and effect of exercise. Diabetes 46: 1775-1781, 1997.
128. Wojtaszewski JF, Jørgensen SB, Frøsig C, MacDonald C, Birk JB, Richter EA. Insulin signalling: effects of prior exercise. Acta Physiol Scand 178: 321-328, 2003.
129. Wojtaszewski JF, Nielsen P, Hansen BF, Richter EA, Kiens B. Isoform-specific and exercise intensity-dependent activation of 5=-AMPactivated protein kinase in human skeletal muscle. J Physiol 528: 221-226, 2000.
130. Wojtaszewski JF, Richter EA. Effects of acute exercise and training on insulin action and sensitivity: focus on molecular mechanisms in muscle. Essays Biochem 42: 31-46, 2006.
131. Yellon DM, Downey JM. Preconditioning the myocardium: from cellular physiology to clinical cardiology. Physiol Rev 83: 1113-1151, 2003.