Intact regulation of the AMPK signaling network in response to exercise and insulin in skeletal muscle of male patients with type 2 diabetes: Illumination of AMPK activation in recovery from exercise

Diabetes

Volumn 65, Issue 5, 2016, Pages 1219-1230

  Kjøbsted, Rasmus ^a   Pedersen, Andreas J T ^b   Hingst, Janne R ^a   Sabaratnam, Rugivan ^b,c   Birk, Jesper B ^a   Kristensen, Jonas M ^b,c   Højlund, Kurt ^b,c   Wojtaszewski, Jørgen F P ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b ODENSE UNIVERSITY HOSPITAL   (Denmark)

^c UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

INSULIN; METFORMIN; SERINE; STRESS ACTIVATED PROTEIN KINASE; SULFONYLUREA; ACACB PROTEIN, HUMAN; ACETYL COENZYME A CARBOXYLASE; ANTIDIABETIC AGENT; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; TBC1D1 PROTEIN, HUMAN; TBC1D4 PROTEIN, HUMAN;

ADAPTATION; ARTICLE; CLINICAL ARTICLE; COMPLEX FORMATION; EXERCISE; EXERCISE RECOVERY; HUMAN; HUMAN TISSUE; HYPERINSULINEMIC-EUGLYCEMIC CLAMP TECHNIQUE; MALE; MUSCLE BIOPSY; MUSCLE METABOLISM; NON INSULIN DEPENDENT DIABETES MELLITUS; OBESITY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; BIOPSY; BODY MASS; COHORT ANALYSIS; COMPLICATION; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; CYCLING; DIABETES MELLITUS, TYPE 2; DRUG EFFECTS; FATIGUE; METABOLISM; MIDDLE AGED; MULTIMODALITY CANCER THERAPY; OVERWEIGHT; PATHOLOGY; PATHOPHYSIOLOGY; PHOSPHORYLATION; PROTEIN PROCESSING; QUADRICEPS FEMORIS MUSCLE;

ACETYL-COA CARBOXYLASE; AMP-ACTIVATED PROTEIN KINASES; BICYCLING; BIOPSY; BODY MASS INDEX; COHORT STUDIES; COMBINED MODALITY THERAPY; DIABETES MELLITUS, TYPE 2; EXERCISE; FATIGUE; GTPASE-ACTIVATING PROTEINS; HUMANS; HYPOGLYCEMIC AGENTS; INSULIN; MALE; MIDDLE AGED; MUSCLE, SKELETAL; OBESITY; OVERWEIGHT; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; QUADRICEPS MUSCLE; SIGNAL TRANSDUCTION;

EID: 84964692024     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db15-1034     Document Type: Article

References (56)

1. Hardie DG. AMPK: a target for drugs and natural products with effects on both diabetes and cancer. Diabetes 2013;62:2164-2172
2. Richter EA, Ruderman NB. AMPK and the biochemistry of exercise: implications for human health and disease. Biochem J 2009;418:261-275
3. Jørgensen SB, Wojtaszewski JFP, Viollet B, et al. Effects of alpha-AMPK knockout on exercise-induced gene activation in mouse skeletal muscle. FASEB J 2005;19:1146-1148
4. Fentz J, Kjøbsted R, Kristensen CM, et al. AMPKa is essential for acute exercise-induced gene responses but not for exercise training-induced adaptations in mouse skeletal muscle. Am J Physiol Endocrinol Metab 2015;309:E900-E914
5. Kjøbsted R, Treebak JT, Fentz J, et al. Prior AICAR stimulation increases insulin sensitivity in mouse skeletal muscle in an AMPK-dependent manner. Diabetes 2015;64:2042-2055
6. Højlund K, Mustard KJ, Staehr P, et al. AMPK activity and isoform protein expression are similar in muscle of obese subjects with and without type 2 diabetes. Am J Physiol Endocrinol Metab 2004;286:E239-E244
7. Wojtaszewski JF, Birk JB, Frøsig C, Holten M, Pilegaard H, Dela F. 5'AMP activated protein kinase expression in human skeletal muscle: effects of strength training and type 2 diabetes. J Physiol 2005;564:563-573
8. Sriwijitkamol A, Coletta DK, Wajcberg E, et al. Effect of acute exercise on AMPK signaling in skeletal muscle of subjects with type 2 diabetes: a timecourse and dose-response study. Diabetes 2007;56:836-848
9. Musi N, Fujii N, Hirshman MF, et al. AMP-activated protein kinase (AMPK) is activated in muscle of subjects with type 2 diabetes during exercise. Diabetes 2001;50:921-927
10. De Filippis E, Alvarez G, Berria R, et al. Insulin-resistant muscle is exercise resistant: evidence for reduced response of nuclear-encoded mitochondrial genes to exercise. Am J Physiol Endocrinol Metab 2008;294:E607-E614
11. Birk JB, Wojtaszewski JFP. Predominant alpha2/beta2/gamma3 AMPK activation during exercise in human skeletal muscle. J Physiol 2006;577:1021-1032
12. Mortensen B, Hingst JR, Frederiksen N, et al. Effect of birth weight and 12 weeks of exercise training on exercise-induced AMPK signaling in human skeletal muscle. Am J Physiol Endocrinol Metab 2013;304:E1379-E1390
13. Cartee GD, Wojtaszewski JFP. Role of Akt substrate of 160 kDa in insulinstimulated and contraction-stimulated glucose transport. Appl Physiol Nutr Metab 2007;32:557-566
14. Taylor EB, An D, Kramer HF, et al. Discovery of TBC1D1 as an insulin-, AICAR-, and contraction-stimulated signaling nexus in mouse skeletal muscle. J Biol Chem 2008;283:9787-9796
15. Pehmøller C, Treebak JT, Birk JB, et al. Genetic disruption of AMPK signaling abolishes both contraction- and insulin-stimulated TBC1D1 phosphorylation and 14-3-3 binding in mouse skeletal muscle. Am J Physiol Endocrinol Metab 2009;297:E665-E675
16. Kramer HF, Witczak CA, Fujii N, et al. Distinct signals regulate AS160 phosphorylation in response to insulin, AICAR, and contraction in mouse skeletal muscle. Diabetes 2006;55:2067-2076
17. Kramer HF, Witczak CA, Taylor EB, Fujii N, Hirshman MF, Goodyear LJ. AS160 regulates insulin- and contraction-stimulated glucose uptake in mouse skeletal muscle. J Biol Chem 2006;281:31478-31485
18. Karlsson HKR, Zierath JR, Kane S, Krook A, Lienhard GE, Wallberg-Henriksson H. Insulin-stimulated phosphorylation of the Akt substrate AS160 is impaired in skeletal muscle of type 2 diabetic subjects. Diabetes 2005;54:1692-1697
19. Middelbeek RJW, Chambers MA, Tantiwong P, et al. Insulin stimulation regulates AS160 and TBC1D1 phosphorylation sites in human skeletal muscle. Nutr Diabetes 2013;3:e74
20. Vind BF, Pehmøller C, Treebak JT, et al. Impaired insulin-induced sitespecific phosphorylation of TBC1 domain family, member 4 (TBC1D4) in skeletal muscle of type 2 diabetes patients is restored by endurance exercise-training. Diabetologia 2011;54:157-167
21. Treebak JT, Frøsig C, Pehmøller C, et al. Potential role of TBC1D4 in enhanced post-exercise insulin action in human skeletal muscle. Diabetologia 2009;52:891-900
22. Pehmøller C, Brandt N, Birk JB, et al Exercise alleviates lipid-induced insulin resistance in human skeletal muscle-signaling interaction at the level of TBC1 domain family member 4. Diabetes 2012;61:2743-2752
23. 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 2007;292:E1191-E1200
24. Frøsig C, Pehmøller C, Birk JB, Richter EA, Wojtaszewski JF. Exerciseinduced TBC1D1 Ser237 phosphorylation and 14-3-3 protein binding capacity in human skeletal muscle. J Physiol 2010;588:4539-4548
25. Treebak JT, Pehmøller C, Kristensen JM, et al. Acute exercise and physiological insulin induce distinct phosphorylation signatures on TBC1D1 and TBC1D4 proteins in human skeletal muscle. J Physiol 2014;592:351-375
26. Jessen N, An D, Lihn AS, et al. Exercise increases TBC1D1 phosphorylation in human skeletal muscle. Am J Physiol Endocrinol Metab 2011;301:E164-E171
27. An D, Toyoda T, Taylor EB, et al. TBC1D1 regulates insulin- and contraction-induced glucose transport in mouse skeletal muscle. Diabetes 2010;59:1358-1365
28. Martin IK, Katz A, Wahren J. Splanchnic and muscle metabolism during exercise in NIDDM patients. Am J Physiol 1995;269:E583-E590
29. Hansen JS, Zhao X, Irmler M, et al. Type 2 diabetes alters metabolic and transcriptional signatures of glucose and amino acid metabolism during exercise and recovery. Diabetologia 2015;58:1845-1854
30. Kingwell BA, Formosa M, Muhlmann M, Bradley SJ, McConell GK. Nitric oxide synthase inhibition reduces glucose uptake during exercise in individuals with type 2 diabetes more than in control subjects. Diabetes 2002;51:2572-2580
31. Pedersen AJT, Hingst JR, Friedrichsen M, Kristensen JM, Højlund K, Wojtaszewski JF. Dysregulation of muscle glycogen synthase in recovery from exercise in type 2 diabetes. Diabetologia 2015;58:1569-1578
32. Kristensen JM, Skov V, Petersson SJ, et al. A PGC-1a- and muscle fibre type-related decrease in markers of mitochondrial oxidative metabolism in skeletal muscle of humans with inherited insulin resistance. Diabetologia 2014;57:1006-1015
33. Jäger S, Handschin C, St-Pierre J, Spiegelman BM. AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1alpha. Proc Natl Acad Sci U S A 2007;104:12017-12022
34. Vind BF, Birk JB, Vienberg SG, et al. Hyperglycaemia normalises insulin action on glucose metabolism but not the impaired activation of AKT and glycogen synthase in the skeletal muscle of patients with type 2 diabetes. Diabetologia 2012;55:1435-1445
35. Højlund K, Birk JB, Klein DK, et al. Dysregulation of glycogen synthase COOH- and NH2-terminal phosphorylation by insulin in obesity and type 2 diabetes mellitus. J Clin Endocrinol Metab 2009;94:4547-4556
36. Stephens NA, Sparks LM. Resistance to the beneficial effects of exercise in type 2 diabetes: are some individuals programmed to fail? J Clin Endocrinol Metab 2015;100:43-52
37. Hussey SE, McGee SL, Garnham A, McConell GK, Hargreaves M. Exercise increases skeletal muscle GLUT4 gene expression in patients with type 2 diabetes. Diabetes Obes Metab 2012;14:768-771
38. Lee-Young RS, Koufogiannis G, Canny BJ, McConell GK. Acute exercise does not cause sustained elevations in AMPK signaling or expression. Med Sci Sports Exerc 2008;40:1490-1494
39. Costford SR, Kavaslar N, Ahituv N, et al. Gain-of-function R225W mutation in human AMPKgamma (3) causing increased glycogen and decreased triglyceride in skeletal muscle. PLoS One 2007;2:e903
40. Milan D, Jeon JT, Looft C, et al. A mutation in PRKAG3 associated with excess glycogen content in pig skeletal muscle. Science 2000;288:1248-1251
41. Barnes BR, Marklund S, Steiler TL, et al. The 59-AMP-activated protein kinase gamma3 isoform has a key role in carbohydrate and lipid metabolism in glycolytic skeletal muscle. J Biol Chem 2004;279:38441-38447
42. Schönke M, Myers MG Jr, Zierath JR, Björnholm M. Skeletal muscle AMPactivated protein kinase g1 (H151R) overexpression enhances whole body energy homeostasis and insulin sensitivity. Am J Physiol Endocrinol Metab 2015;309:E679-E690
43. Garcia-Roves PM, Osler ME, Holmström MH, Zierath JR. Gain-of-function R225Q mutation in AMP-activated protein kinase gamma3 subunit increases mitochondrial biogenesis in glycolytic skeletal muscle. J Biol Chem 2008;283:35724-35734
44. Wu Z, Puigserver P, Andersson U, et al. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 1999;98:115-124
45. Vichaiwong K, Purohit S, An D, et al. Contraction regulates sitespecific phosphorylation of TBC1D1 in skeletal muscle. Biochem J 2010;431:311-320
46. Stöckli J, Meoli CC, Hoffman NJ, et al. The RabGAP TBC1D1 plays a central role in exercise-regulated glucose metabolism in skeletal muscle. Diabetes 2015;64:1914-1922
47. Kennedy JW, Hirshman MF, Gervino EV, et al. Acute exercise induces GLUT4 translocation in skeletal muscle of normal human subjects and subjects with type 2 diabetes. Diabetes 1999;48:1192-1197
48. Fentz J, Kjøbsted R, Birk JB, et al. AMPKa is critical for enhancing skeletal muscle fatty acid utilization during in vivo exercise in mice. FASEB J 2015;29:1725-1738
49. Nordsborg NB, Lundby C, Leick L, Pilegaard H. Relative workload determines exercise-induced increases in PGC-1alpha mRNA. Med Sci Sports Exerc 2010;42:1477-1484
50. 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 2009;297:E242-E251
51. Frøsig C, Sajan MP, Maarbjerg SJ, et al. 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 2007;582:1289-1301
52. Wojtaszewski JF, Hansen BF, Gade J, et al. Insulin signaling and insulin sensitivity after exercise in human skeletal muscle. Diabetes 2000;49:325-331
53. Devlin JT, Hirshman M, Horton ED, Horton ES. Enhanced peripheral and splanchnic insulin sensitivity in NIDDM men after single bout of exercise. Diabetes 1987;36:434-439
54. Højlund K, Staehr P, Hansen BF, et al. Increased phosphorylation of skeletal muscle glycogen synthase at NH2-terminal sites during physiological hyperinsulinemia in type 2 diabetes. Diabetes 2003;52:1393-1402
55. 13C nuclear magnetic resonance spectroscopy. N Engl J Med 1990;322:223-228
56. Jørgensen SB, Nielsen JN, Birk JB, et al. The a2-5'AMP-activated protein kinase is a site 2 glycogen synthase kinase in skeletal muscle and is responsive to glucose loading. Diabetes 2004;53:3074-3081