Prolonged exercise training increases intramuscular lipid content and perilipin 2 expression in type I muscle fibers of patients with type 2 diabetes

American Journal of Physiology - Endocrinology and Metabolism

Volumn 303, Issue 9, 2012, Pages

  Shaw, C S ^a,b   Shepherd, S O ^a   Wagenmakers, A J M ^a   Hansen, D ^c,d   Dendale, P ^c,d   van Loon, L J C ^e  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b VICTORIA UNIVERSITY   (Australia)

^c JESSA HOSPITAL   (Belgium)

^d HASSELT UNIVERSITY   (Belgium)

^e MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Adipocyte differentiation related protein; Adipophilin; Insulin sensitivity; Intramuscular triglyceride; Lipid metabolism

Indexed keywords

PERILIPIN; PERILIPIN 2; TRIACYLGLYCEROL; UNCLASSIFIED DRUG;

ADULT; ARTICLE; BODY MASS; CLINICAL ARTICLE; ENDURANCE TRAINING; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MALE; MUSCLE BIOPSY; MUSCLE CELL; MUSCLE FIBER TYPE 1; MUSCLE LEVEL; NON INSULIN DEPENDENT DIABETES MELLITUS; OBESITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKELETAL MUSCLE;

ABDOMINAL FAT; ADIPOSITY; BODY MASS INDEX; COHORT STUDIES; DIABETES MELLITUS, TYPE 2; EXERCISE; HUMANS; INSULIN RESISTANCE; LIPID METABOLISM; MALE; MEMBRANE PROTEINS; MIDDLE AGED; MITOCHONDRIA, MUSCLE; MUSCLE FIBERS, FAST-TWITCH; MUSCLE FIBERS, SLOW-TWITCH; OVERWEIGHT; OXYGEN CONSUMPTION; QUADRICEPS MUSCLE; TIME FACTORS; TRIGLYCERIDES;

EID: 84868326874     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00272.2012     Document Type: Article

References (48)

1. Bell M, Wang H, Chen H, McLenithan JC, Gong DW, Yang RZ, Yu D, Fried SK, Quon MJ, Londos C, Sztalryd C. Consequences of lipid droplet coat protein downregulation in liver cells: abnormal lipid droplet metabolism and induction of insulin resistance. Diabetes 57: 2037-2045, 2008.
2. Boushel R, Gnaiger E, Schjerling P, Skovbro M, Kraunsøe R, Dela F. Patients with type 2 diabetes have normal mitochondrial function in skeletal muscle. Diabetologia 50: 790-796, 2007.
3. Brasaemle D, Barber T, Wolins N, Serrero G, Blanchette-Mackie E, Londos C. Adipose differentiation-related protein is an ubiquitously expressed lipid storage droplet-associated protein. J Lipid Res 38: 2249-2263, 1997.
4. Bruce C, Kriketos A, Cooney G, Hawley J. Disassociation of muscle triglyceride content and insulin sensitivity after exercise training in patients with type 2 diabetes. Diabetologia 47: 23-30, 2004.
5. Bruce CR, Anderson MJ, Carey AL, Newman DG, Bonen A, Kriketos AD, Cooney GJ, Hawley JA. Muscle oxidative capacity is a better predictor of insulin sensitivity than lipid status. J Clin Endocrinol Metab 88: 5444-5451, 2003.
6. Bruce CR, Thrush AB, Mertz VA, Bezaire V, Chabowski A, Heigenhauser GJ, Dyck DJ. Endurance training in obese humans improves glucose tolerance and mitochondrial fatty acid oxidation and alters muscle lipid content. Am J Physiol Endocrinol Metab 291: E99-E107, 2006.
7. Church TS, Blair SN, Cocreham S, Johannsen N, Johnson W, Kramer K, Mikus CR, Myers V, Nauta M, Rodarte RQ, Sparks L, Thompson A, Earnest CP. Effects of aerobic and resistance training on hemoglobin A1c levels in patients with type 2 diabetes: a randomized controlled trial. JAMA 304: 2253-2262, 2010.
8. Coen PM, Dubé JJ, Amati F, Stefanovic-Racic M, Ferrell RE, Toledo FG, Goodpaster BH. Insulin resistance is associated with higher intramyocellular triglycerides in type I but not type II myocytes concomitant with higher ceramide content. Diabetes 59: 80-88, 2010.
9. Dubé JJ, Amati F, Toledo FG, Stefanovic-Racic M, Rossi A, Coen P, Goodpaster BH. Effects of weight loss and exercise on insulin resistance, and intramyocellular triacylglycerol, diacylglycerol and ceramide. Diabetologia 54: 1147-1156, 2011.
10. Dubé JJ, Amati F, Stefanovic-Racic M, Toledo FG, Sauers SE, Goodpaster BH. Exercise-induced alterations in intramyocellular lipids and insulin resistance: the athlete's paradox revisited. Am J Physiol Endocrinol Metab 294: E882-E888, 2008.
11. Farese RV Jr, Walther TC. Lipid droplets finally get a little R-E-S-PE-C-T. Cell 139: 855-860, 2009.
12. Goodman JM. The gregarious lipid droplet. J Biol Chem 283: 28005-28009, 2008.
13. Goodpaster BH, He J, Watkins S, Kelley DE. Skeletal muscle lipid content and insulin resistance: evidence for a paradox in endurance-trained athletes. J Clin Endocrinol Metab 86: 5755-5761, 2001.
14. Goodpaster BH, Katsiaras A, Kelley DE. Enhanced fat oxidation through physical activity is associated with improvements in insulin sensitivity in obesity. Diabetes 52: 2191-2197, 2003.
15. Granneman JG, Moore HP, Krishnamoorthy R, Rathod M. Perilipin controls lipolysis by regulating the interactions of AB-hydrolase containing 5 (Abhd5) and adipose triglyceride lipase (Atgl). J Biol Chem 284: 34538, 2009.
16. Hansen D, Dendale P, Jonkers RA, Beelen M, Manders RJ, Corluy L, Mullens A, Berger J, Meeusen R, van Loon LJ. Continuous low-to moderate-intensity exercise training is as effective as moderate-to highintensity exercise training at lowering blood HbA(1c) in obese type 2 diabetes patients. Diabetologia 52: 1789-1797, 2009.
17. Hansen D, Dendale P, van Loon LJ, Meeusen R. The impact of training modalities on the clinical benefits of exercise intervention in patients with cardiovascular disease risk or type 2 diabetes mellitus. Sports Med 40: 921-940, 2010.
18. Hey-Mogensen M, Højlund K, Vind B, Wang L, Dela F, Beck-Nielsen H, Fernström M, Sahlin K. 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, 2010.
19. Kelley DE, Goodpaster B, Wing RR, Simoneau JA. Skeletal muscle fatty acid metabolism in association with insulin resistance, obesity, and weight loss. Am J Physiol Endocrinol Metab 277: E1130-E1141, 1999.
20. Kelley DE, He J, Menshikova EV, Ritov VB. Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 51: 2944-2950, 2002.
21. Kelley DE, Simoneau JA. Impaired free fatty acid utilization by skeletal muscle in non-insulin-dependent diabetes mellitus. J Clin Invest 94: 2349-2356, 1994.
22. Kimmel AR, Brasaemle DL, McAndrews-Hill M, Sztalryd C, Londos C. Adoption of PERILIPIN as a unifying nomenclature for the mammalian PAT-family of intracellular lipid storage droplet proteins. J Lipid Res 51: 468-471, 2010.
23. Listenberger LL, Ostermeyer-Fay AG, Goldberg EB, Brown WJ, Brown DA. Adipocyte differentiation-related protein reduces the lipid droplet association of adipose triglyceride lipase and slows triacylglycerol turnover. J Lipid Res 48: 2751-2761, 2007.
24. Londos C, Brasaemle DL, Schultz CJ, Segrest JP, Kimmel AR. Perilipins, ADRP, and other proteins that associate with intracellular neutral lipid droplets in animal cells. Semin Cell Dev Biol 10: 51-58, 1999.
25. Manley S. Haemoglobin A1c-a marker for complications of type 2 diabetes: the experience from the UK Prospective Diabetes Study (UKPDS). Clin Chem Lab Med 41: 1182-1190, 2003.
26. Meex RC, Schrauwen-Hinderling VB, Moonen-Kornips E, Schaart G, Mensink M, Phielix E, Van De Weijer T, Sels JP, Schrauwen P, Hesselink MK. Restoration of muscle mitochondrial function and metabolic flexibility in type 2 diabetes by exercise training is paralleled by increased myocellular fat storage and improved insulin sensitivity. Diabetes 59: 572-579, 2010.
27. Minnaard R, Schrauwen P, Schaart G, Jorgensen JA, Lenaers E, Mensink M, Hesselink MK. Adipocyte differentiation-related protein and OXPAT in rat and human skeletal muscle: involvement in lipid accumulation and type 2 diabetes mellitus. J Clin Endocrinol Metab 94: 4077-4085, 2009.
28. Moro C, Bajpeyi S, Smith SR. Determinants of intramyocellular triglyceride turnover: implications for insulin sensitivity. Am J Physiol Endocrinol Metab 294: E203-E213, 2008.
29. Nielsen J, Mogensen M, Vind BF, Sahlin K, Højlund K, Schrøder HD, Ørtenblad N. Increased subsarcolemmal lipids in type 2 diabetes: effect of training on localization of lipids, mitochondria, and glycogen in sedentary human skeletal muscle. Am J Physiol Endocrinol Metab 298: E706-E713, 2010.
30. Pan DA, Lillioja S, Kriketos AD, Milner MR, Baur LA, Bogardus C, Jenkins AB, Storlien LH. Skeletal muscle triglyceride levels are inversely related to insulin action. Diabetes 46: 983-988, 1997.
31. Phielix E, Meex R, Moonen-Kornips E, Hesselink MK, Schrauwen P. Exercise training increases mitochondrial content and ex vivo mitochon-drial function similarly in patients with type 2 diabetes and in control individuals. Diabetologia 53: 1714-1721, 2010.
32. Phillips SA, Choe CC, Ciaraldi TP, Greenberg AS, Kong AP, Baxi SC, Christiansen L, Mudaliar SR, Henry RR. Adipocyte differentiationrelated protein in human skeletal muscle: relationship to insulin sensitivity. Obes Res 13: 1321-1329, 2005.
33. Praet SF, van Loon LJ. Optimizing the therapeutic benefits of exercise in Type 2 diabetes. J Appl Physiol 103: 1113-1120, 2007.
34. Prats C, Donsmark M, Qvortrup K, Londos C, Sztalryd C, Holm C, Galbo H, Ploug T. Decrease in intramuscular lipid droplets and translocation of HSL in response to muscle contraction and epinephrine. J Lipid Res 47: 2392-2399, 2006.
35. Pruchnic R, Katsiaras A, He J, Kelley DE, Winters C, Goodpaster BH. Exercise training increases intramyocellular lipid and oxidative capacity in older adults. Am J Physiol Endocrinol Metab 287: E857-E862, 2004.
36. Ritov VB, Menshikova EV, He J, Ferrell RE, Goodpaster BH, Kelley DE. Deficiency of subsarcolemmal mitochondria in obesity and type 2 diabetes. Diabetes 54: 8-14, 2005.
37. 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.
38. Shaw CS, Jones DA, Wagenmakers AJM. Network distribution of mitochondria and lipid droplets in human muscle fibres. Histochem Cell Biol 129: 65-72, 2008.
39. Shaw CS, Sherlock M, Stewart PM, Wagenmakers AJM. Adipophilin distribution and colocalisation with lipid droplets in skeletal muscle. Histochem Cell Biol 131: 575-581, 2009.
40. Shepherd SO, Cocks M, Tipton KD, Ranasinghe AM, Barker TA, Burniston JG, Wagenmakers AJ, Shaw CS. Preferential utilization of perilipin 2-associated intramuscular triglycerides during 1 h of moderateintensity endurance-type exercise. Exp Physiol 97: 970-980, 2012.
41. Short KR, Vittone JL, Bigelow ML, Proctor DN, Rizza RA, Coenen-Schimke JM, Nair KS. Impact of aerobic exercise training on age-related changes in insulin sensitivity and muscle oxidative capacity. Diabetes 52: 1888-1896, 2003.
42. Solomon TP, Sistrun SN, Krishnan RK, Del Aguila LF, Marchetti CM, O'Carroll SM, O'Leary VB, Kirwan JP. Exercise and diet enhance fat oxidation and reduce insulin resistance in older obese adults. J Appl Physiol 104: 1313-1319, 2008.
43. Stellingwerff T, Boon H, Jonkers RA, Senden JM, Spriet LL, Koopman R, van Loon LJ. Significant intramyocellular lipid use during prolonged cycling in endurance-trained males as assessed by three different methodologies. Am J Physiol Endocrinol Metab 292: E1715-E1723, 2007.
44. Tarnopolsky MA, Rennie CD, Robertshaw HA, Fedak-Tarnopolsky SN, Devries MC, Hamadeh MJ. Influence of endurance exercise training and sex on intramyocellular lipid and mitochondrial ultrastructure, substrate use, and mitochondrial enzyme activity. Am J Physiol Regul Integr Comp Physiol 292: R1271-R1278, 2007.
45. van Loon LJ. Use of intramuscular triacylglycerol as a substrate source during exercise in humans. J Appl Physiol 97: 1170-1187, 2004.
46. van Loon LJ, Koopman R, Manders R, van der Weegen W, van Kranenburg GP, Keizer HA. Intramyocellular lipid content in type 2 diabetes patients compared with overweight sedentary men and highly trained endurance athletes. Am J Physiol Endocrinol Metab 287: E558-E565, 2004.
47. van Loon LJ, Koopman R, Stegen JH, Wagenmakers AJ, Keizer HA, Saris WH. Intramyocellular lipids form an important substrate source during moderate intensity exercise in endurance-trained males in a fasted state. J Physiol 553: 611-625, 2003.
48. Wang H, Hu L, Dalen K, Dorward H, Marcinkiewicz A, Russell D, Gong D, Londos C, Yamaguchi T, Holm C. Activation of hormonesensitive lipase requires two steps, protein phosphorylation and binding to the PAT-1 domain of lipid droplet coat proteins. J Biol Chem 284: 32116-32125, 2009.