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

Volumn 54, Issue 1, 2011, Pages 157-167

  Vind, B F ^a   Pehmoller C ^b   Treebak, J T ^b   Birk, J B ^b   Hey Mogensen, M ^c   Beck Nielsen, H ^a   Zierath, J R ^d   Wojtaszewski, J F P ^b   Hojlund K ^a  

^a ODENSE UNIVERSITY HOSPITAL   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^d KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Akt; Exercise training; Glycogen synthase; Insulin signalling; TBC1D4; Type 2 diabetes

Indexed keywords

ADENYLATE KINASE; GLUCOSE TRANSPORTER 4; GLYCOGEN SYNTHASE; HEXOKINASE; HEXOKINASE 2; INSULIN; PROTEIN KINASE B; PROTEIN KINASE B BETA; REGULATOR PROTEIN; TBC1 DOMAIN FAMILY MEMBER 4 PROTEIN; UNCLASSIFIED DRUG;

ADULT; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; ENDURANCE TRAINING; GLUCOSE TRANSPORT; HUMAN; HUMAN TISSUE; MALE; NON INSULIN DEPENDENT DIABETES MELLITUS; OBESITY; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; VASTUS LATERALIS MUSCLE;

BLOOD GLUCOSE; BLOTTING, WESTERN; C-PEPTIDE; DIABETES MELLITUS, TYPE 2; ELECTROPHORESIS, POLYACRYLAMIDE GEL; EXERCISE; GLUCOSE CLAMP TECHNIQUE; GLYCOGEN SYNTHASE; GTPASE-ACTIVATING PROTEINS; HEMOGLOBIN A, GLYCOSYLATED; HUMANS; INSULIN; MALE; MIDDLE AGED; MUSCLE, SKELETAL; PHOSPHORYLATION;

EID: 79953767747     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-010-1924-4     Document Type: Article

References (48)

1. Højlund K, 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
2. Taniguchi CM, Emanuelli B, Kahn CR (2006) Critical nodes in signalling pathways: insights into insulin action. Nat Rev Mol Cell Biol 7:85-96 (Pubitemid 43278292) (Pubitemid 43278292)
3. Kane S, Sano H, Liu SC et al (2002) A method to identify serine kinase substrates. Akt phosphorylates a novel adipocyte protein with a Rab GTPase-activating protein (GAP) domain. J Biol Chem 277:22115-22118 (Pubitemid 34967174) (Pubitemid 34967174)
4. Sano H, Kane S, Sano E et al (2003) Insulin-stimulated phosphorylation of a Rab GTPase-activating protein regulates GLUT4 translocation. J Biol Chem 278:14599-14602 (Pubitemid 36799780) (Pubitemid 36799780)
5. Kramer HF, Witczak CA, Taylor EB, Fujii N, Hirshman MF, Goodyear LJ (2006) AS160 regulates insulin- and contraction-stimulated glucose uptake in mouse skeletal muscle. J Biol Chem 281:31478-31485 (Pubitemid 46041412) (Pubitemid 46041412)
6. Geraghty KM, Chen S, Harthill JE et al (2007) Regulation of multisite phosphorylation and 14-3-3 binding of AS160 in response to IGF-1, EGF, PMA and AICAR. Biochem J 407:231-241 (Pubitemid 47556988) (Pubitemid 47556988)
7. Treebak JT, Taylor EB, Witczak CA et al (2010) Identification of a novel phosphorylation site on TBC1D4 regulated by AMP-activated protein kinase in skeletal muscle. Am J Physiol Cell Physiol 298:C377-C385
8. Ramm G, Larance M, Guilhaus M, James DE (2006) A role for 14-3-3 in insulin-stimulated GLUT4 translocation through its interaction with the RabGAP AS160. J Biol Chem 281:29174-29180 (Pubitemid 44507061) (Pubitemid 44507061)
9. Cartee GD, Wojtaszewski JF (2007) Role of Akt substrate of 160 kDa in insulin-stimulated and contraction-stimulated glucose transport. Appl Physiol Nutr Metab 32:557-566
10. Wojtaszewski JF, Richter EA (2006) Effects of acute exercise and training on insulin action and sensitivity: focus on molecular mechanisms in muscle. Essays Biochem 42:31-46
11. Frøsig C, Rose AJ, Treebak JT, Kiens B, Richter EA,Wojtaszewski JFP (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 (Pubitemid 47195824) (Pubitemid 47195824)
12. Treebak JT, Frosig C, Pehmoller C et al (2009) Potential role of TBC1D4 in enhanced post-exercise insulin action in human skeletal muscle. Diabetologia 52:891-900
13. Treebak JT, Birk JB, Rose AJ, Kiens B, Richter EA, Wojtaszewski JF (2007) AS160 phosphorylation is associated with activation of alpha2beta2gamma1- but not alpha2beta2gamma3-AMPK trimeric complex in skeletal muscle during exercise in humans. Am J Physiol Endocrinol Metab 292:E715-E722
14. Treebak JT, Wojtaszewski JF (2008) Role of 5'AMP-activated protein kinase in skeletal muscle. Int J Obes (Lond) 32(Suppl 4): S13-S17
15. Højlund K, Staehr P, Hansen BF et al (2003) Increased phosphorylation of skeletal muscle glycogen synthase at NH2-terminal sites during physiological hyperinsulinemia in type 2 diabetes. Diabetes 52:1393-1402 (Pubitemid 36666193) (Pubitemid 36666193)
16. Damsbo P, Vaag A, Hother-Nielsen O, Beck-Nielsen H (1991) Reduced glycogen synthase activity in skeletal muscle from obese patients with and without type 2 (non-insulin-dependent) diabetes mellitus. Diabetologia 34:239-245
17. Cusi K, Maezono K, Osman A et al (2000) Insulin resistance differentially affects the PI 3-kinase- and MAP kinase-mediated signaling in human muscle. J Clin Invest 105:311-320 (Pubitemid 30094451) (Pubitemid 30094451)
18. Højlund K, Wojtaszewski JF, Birk J, Hansen BF, Vestergaard H, Beck-Nielsen H (2006) Partial rescue of in vivo insulin signalling in skeletal muscle by impaired insulin clearance in heterozygous carriers of a mutation in the insulin receptor gene. Diabetologia 49:1827-1837 (Pubitemid 44025037) (Pubitemid 44025037)
19. Glintborg D, Højlund K, Andersen NR, Falck-Hansen B, Beck-Nielsen H, Wojtaszewski JFP (2008) Impaired insulin activation and dephosphorylation of glycogen synthase in skeletal muscle of women with polycystic ovary syndrome is reversed by pioglitazone treatment. J Clin Endocrinol Metab 93:3618-3626
20. Karlsson HK, Ahlsen M, Zierath JR, Wallberg-Henriksson H, Koistinen HA (2006) Insulin signaling and glucose transport in skeletal muscle from first-degree relatives of type 2 diabetic patients. Diabetes 55:1283-1288 (Pubitemid 44195366) (Pubitemid 44195366)
21. O'Gorman DJ, Karlsson HK, McQuaid S et al (2006) Exercise training increases insulin-stimulated glucose disposal and GLUT4 (SLC2A4) protein content in patients with type 2 diabetes. Diabetologia 49:2983-2992 (Pubitemid 44730302) (Pubitemid 44730302)
22. Beeson M, Sajan MP, Dizon M et al (2003) Activation of protein kinase C-zeta by insulin and phosphatidylinositol-3, 4, 5-(PO4)3 is defective in muscle in type 2 diabetes and impaired glucose tolerance: amelioration by rosiglitazone and exercise. Diabetes 52:1926-1934 (Pubitemid 36919783) (Pubitemid 36919783)
23. Bandyopadhyay GK, Yu JG, Ofrecio J, Olefsky JM (2005) Increased p85/55/50 expression and decreased phosphotidylinositol 3-kinase activity in insulin-resistant human skeletal muscle. Diabetes 54:2351-2359 (Pubitemid 41134262)
24. Højlund K, Birk JB, Klein DK et al (2009) Dysregulation of glycogen synthase COOH- and NH2-terminal phosphorylation by insulin in obesity and type 2 diabetes mellitus. J Clin Endocrinol Metab 94:4547-4556
25. Karlsson HK, Zierath JR, Kane S, Krook A, Lienhard GE, Wallberg-Henriksson H (2005) Insulin-stimulated phosphorylation of the Akt substrate AS160 is impaired in skeletal muscle of type 2 diabetic subjects. Diabetes 54:1692-1697 (Pubitemid 40770759)
26. Højlund K, Glintborg D, Andersen NR et al (2008) Impaired insulin-stimulated phosphorylation of Akt and AS160 in skeletal muscle of women with polycystic ovary syndrome is reversed by pioglitazone treatment. Diabetes 57:357-366
27. Adams JM II, Pratipanawatr T, Berria R et al (2004) Ceramide content is increased in skeletal muscle from obese insulin-resistant humans. Diabetes 53:25-31 (Pubitemid 38044694) (Pubitemid 38044694)
28. Morino K, Petersen KF, Dufour S et al (2005) Reduced mitochondrial density and increased IRS-1 serine phosphorylation in muscle of insulin-resistant offspring of type 2 diabetic parents. J Clin Invest 115:3587-3593 (Pubitemid 43121847) (Pubitemid 43121847)
29. Tuomilehto J, Lindstrom J, Eriksson JG et al (2001) Prevention of type 2 diabetes mellitus by changes in lifestyle among subjects with impaired glucose tolerance. N Engl J Med 344:1343-1350 (Pubitemid 32378388) (Pubitemid 32378388)
30. Knowler WC, Barrett-Connor E, Fowler SE et al (2002) Reduction in the incidence of type 2 diabetes with lifestyle intervention or metformin. N Engl J Med 346:393-403 (Pubitemid 34437694) (Pubitemid 34437694)
31. Wang Y, Simar D, Fiatarone Singh MA (2009) Adaptations to exercise training within skeletal muscle in adults with type 2 diabetes or impaired glucose tolerance: a systematic review. Diabetes Metab Res Rev 25:13-40
32. Christ-Roberts CY, Pratipanawatr T, Pratipanawatr W et al (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 (Pubitemid 39140763) (Pubitemid 39140763)
33. Daugaard JR, Richter EA (2001) Relationship between muscle fibre composition, glucose transporter protein 4 and exercise training: possible consequences in non-insulin-dependent diabetes mellitus. Acta Physiol Scand 171:267-276 (Pubitemid 32825511) (Pubitemid 32825511)
34. Mogensen M, Vind BF, Højlund K, Beck-Nielsen H, Sahlin K (2009) Maximal lipid oxidation in patients with type 2 diabetes is normal and shows an adequate increase in response to aerobic training. Diabetes Obes Metab 11:874-883
35. Hey-Mogensen M, Højlund K, Vind BF et al (2009) Effect of physical training on mitochondrial respiration and reactive oxygen species release in skeletal muscle in patients with obesity and type 2 diabetes. Diabetologia 53:1976-1985
36. Birk JB, Wojtaszewski JF (2006) Predominant alpha2/beta2/ gamma3 AMPK activation during exercise in human skeletal muscle. J Physiol 577:1021-1032 (Pubitemid 44873663) (Pubitemid 44873663)
37. Deshmukh A, Coffey VG, Zhong Z, Chibalin AV, Hawley JA, Zierath JR (2006) Exercise-induced phosphorylation of the novel akt substrates AS160 and filamin A in human skeletal muscle. Diabetes 55:1776-1782 (Pubitemid 44324132) (Pubitemid 44324132)
38. Treebak JT, Glund S, Deshmukh A et al (2006) AMPK-mediated AS160 phosphorylation in skeletal muscle is dependent on AMPK catalytic and regulatory subunits. Diabetes 55:2051-2058 (Pubitemid 44509979) (Pubitemid 44509979)
39. Plomgaard P, Bouzakri K, Krogh-Madsen R, Mittendorfer B, Zierath JR, Pedersen BK (2005) Tumor necrosis factor-alpha induces skeletal muscle insulin resistance in healthy human subjects via inhibition of Akt substrate 160 phosphorylation. Diabetes 54:2939-2945 (Pubitemid 41401090) (Pubitemid 41401090)
40. Taylor EB, An D, Kramer HF et al (2008) Discovery of TBC1D1 as an insulin-, AICAR-, and contraction-stimulated signaling nexus in mouse skeletal muscle. J Biol Chem 283:9787-9796
41. Pehmøller C, Treebak JT, Birk JB et al (2009) Genetic disruption of AMPK signaling abolishes both contraction- and insulinstimulated TBC1D1 phosphorylation and 14-3-3 binding in mouse skeletal muscle. Am J Physiol Endocrinol Metab 297: E665-E675
42. Krook A, Roth RA, Jiang XJ, Zierath JR, Wallberg-Henriksson H (1998) Insulin-stimulated Akt kinase activity is reduced in skeletal muscle from NIDDM subjects. Diabetes 47:1281-1286 (Pubitemid 28357006) (Pubitemid 28357006)
43. Højlund K, Frystyk J, Levin K, Flyvbjerg A, Wojtaszewski JFP, Beck-Nielsen H (2006) Reduced plasma adiponectin concentrations may contribute to impaired insulin activation of glycogen synthase in skeletal muscle of patients with type 2 diabetes. Diabetologia 49:1283-1291
44. Vestergaard H, Bjørbaek C, Hansen T, Larsen FS, Granner DK, Pedersen O (1995) Impaired activity and gene expression of hexokinase II in muscle from non-insulin-dependent diabetes mellitus patients. J Clin Invest 96:2639-2645
45. Fisher JS, Gao J, Han DH, Holloszy JO, Nolte LA (2002) Activation of AMP kinase enhances sensitivity of muscle glucose transport to insulin. Am J Physiol Endocrinol Metab 282:E18-E23 (Pubitemid 34654101) (Pubitemid 34654101)
46. Dela F, Larsen JJ, Mikines KJ, Ploug T, Petersen LN, Galbo H (1995) Insulin-stimulated muscle glucose clearance in patients with NIDDM. Effects of one-legged physical training. Diabetes 44:1010-1020
47. Bruce CR, Kriketos AD, Cooney GJ, Hawley JA (2004) Disassociation of muscle triglyceride content and insulin sensitivity after exercise training in patients with type 2 diabetes. Diabetologia 47:23-30 (Pubitemid 38141936)
48. Wasserman DH (2009) Four grams of glucose. Am J Physiol Endocrinol Metab 296:E11-E21