Muscle mitochondria and insulin resistance: A human perspective

Trends in Endocrinology and Metabolism

Volumn 23, Issue 9, 2012, Pages 444-450

  Hoeks, Joris ^a   Schrauwen, Patrick ^a  

^a MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Calorie restriction; Diabetes; Mitochondrial capacity; Resveratrol

Indexed keywords

AEROBIC METABOLISM; ARTICLE; CALORIC RESTRICTION; EXERCISE; HUMAN; INSULIN RESISTANCE; LIPID STORAGE; MITOCHONDRIAL RESPIRATION; MUSCLE METABOLISM; MUSCLE MITOCHONDRION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; DIABETES MELLITUS, TYPE 2; HUMANS; INSULIN RESISTANCE; MITOCHONDRIA, MUSCLE; STILBENES;

EID: 84865405481     PISSN: 10432760     EISSN: 18793061     Source Type: Journal    
DOI: 10.1016/j.tem.2012.05.007     Document Type: Article

References (61)

1. Wild S., et al. Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care 2004, 27:1047-1053.
2. 13C nuclear magnetic resonance spectroscopy. N. Engl. J. Med. 1990, 322:223-228.
3. Bachmann O.P., et al. Effects of intravenous and dietary lipid challenge on intramyocellular lipid content and the relation with insulin sensitivity in humans. Diabetes 2001, 50:2579-2584.
4. Schrauwen-Hinderling V.B., et al. Intramyocellular lipid content and molecular adaptations in response to a 1-week high-fat diet. Obes. Res. 2005, 13:2088-2094.
5. van Herpen N.A., et al. Three weeks on a high-fat diet increases intrahepatic lipid accumulation and decreases metabolic flexibility in healthy overweight men. J. Clin. Endocrinol. Metab. 2011, 96:E691-E695.
6. 1H NMR spectroscopy study. Diabetologia 1999, 42:113-116.
7. 13C nuclear magnetic resonance spectroscopy assessment in offspring of type 2 diabetic parents. Diabetes 1999, 48:1600-1606.
8. Blaak E.E., et al. Impaired oxidation of plasma-derived fatty acids in type 2 diabetic subjects during moderate-intensity exercise. Diabetes 2000, 49:2102-2107.
9. Mensink M., et al. Plasma free fatty acid uptake and oxidation are already diminished in subjects at high risk for developing type 2 diabetes. Diabetes 2001, 50:2548-2554.
10. Simoneau J.A., et al. Markers of capacity to utilize fatty acids in human skeletal muscle: relation to insulin resistance and obesity and effects of weight loss. FASEB J. 1999, 13:2051-2060.
11. Simoneau J.A., Kelley D.E. Altered glycolytic and oxidative capacities of skeletal muscle contribute to insulin resistance in NIDDM. J. Appl. Physiol. 1997, 83:166-171.
12. Kelley D.E., et al. Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 2002, 51:2944-2950.
13. Mootha V.K., et al. PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat. Genet. 2003, 34:267-273.
14. Patti M.E., et al. Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: potential role of PGC1 and NRF1. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:8466-8471.
15. Skov V., et al. Reduced expression of nuclear-encoded genes involved in mitochondrial oxidative metabolism in skeletal muscle of insulin-resistant women with polycystic ovary syndrome. Diabetes 2007, 56:2349-2355.
16. Hwang H., et al. Proteomics analysis of human skeletal muscle reveals novel abnormalities in obesity and type 2 diabetes. Diabetes 2010, 59:33-42.
17. Petersen K.F., et al. Mitochondrial dysfunction in the elderly: possible role in insulin resistance. Science 2003, 300:1140-1142.
18. Petersen K.F., et al. Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N. Engl. J. Med. 2004, 350:664-671.
19. Befroy D.E., et al. Impaired mitochondrial substrate oxidation in muscle of insulin-resistant offspring of type 2 diabetic patients. Diabetes 2007, 56:1376-1381.
20. Schrauwen-Hinderling V.B., et al. Impaired in vivo mitochondrial function but similar intramyocellular lipid content in patients with type 2 diabetes mellitus and BMI-matched control subjects. Diabetologia 2007, 50:113-120.
21. Ritov V.B., et al. Deficiency of subsarcolemmal mitochondria in obesity and type 2 diabetes. Diabetes 2005, 54:8-14.
22. Morino K., et al. Reduced mitochondrial density and increased IRS-1 serine phosphorylation in muscle of insulin-resistant offspring of type 2 diabetic parents. J. Clin. Invest. 2005, 115:3587-3593.
23. Phielix E., et al. Lower intrinsic ADP-stimulated mitochondrial respiration underlies in vivo mitochondrial dysfunction in muscle of male type 2 diabetic patients. Diabetes 2008, 57:2943-2949.
24. Chomentowski P., et al. Skeletal muscle mitochondria in insulin resistance: differences in intermyofibrillar versus subsarcolemmal subpopulations and relationship to metabolic flexibility. J. Clin. Endocrinol. Metab. 2011, 96:494-503.
25. Ukropcova B., et al. Family history of diabetes links impaired substrate switching and reduced mitochondrial content in skeletal muscle. Diabetes 2007, 56:720-727.
26. Mogensen M., et al. Mitochondrial respiration is decreased in skeletal muscle of patients with type 2 diabetes. Diabetes 2007, 56:1592-1599.
27. Boushel R., et al. Patients with type 2 diabetes have normal mitochondrial function in skeletal muscle. Diabetologia 2007, 50:790-796.
28. Larsen S., et al. Increased mitochondrial substrate sensitivity in skeletal muscle of patients with type 2 diabetes. Diabetologia 2011, 54:1427-1436.
29. Rabol R., et al. Regional anatomic differences in skeletal muscle mitochondrial respiration in type 2 diabetes and obesity. J. Clin. Endocrinol. Metab. 2010, 95:857-863.
30. Meex R.C., et al. 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 2010, 59:572-579.
31. Minet A.D., Gaster M. ATP synthesis is impaired in isolated mitochondria from myotubes established from type 2 diabetic subjects. Biochem. Biophys. Res. Commun. 2010, 402:70-74.
32. Minet A.D., Gaster M. The dynamic equilibrium between ATP synthesis and ATP consumption is lower in isolated mitochondria from myotubes established from type 2 diabetic subjects compared to lean control. Biochem. Biophys. Res. Commun. 2011, 409:591-595.
33. Raubenheimer P.J. Impaired mitochondrial activity and insulin-resistant offspring of patients with type 2 diabetes. N. Engl. J. Med. 2004, 350:2419-2421.
34. Short K.R., et al. Impaired mitochondrial activity and insulin-resistant offspring of patients with type 2 diabetes. N. Engl. J. Med. 2004, 350:2419-2421.
35. Hoeks J., et al. Prolonged fasting identifies skeletal muscle mitochondrial dysfunction as consequence rather than cause of human insulin resistance. Diabetes 2010, 59:2117-2125.
36. Stump C.S., et al. Effect of insulin on human skeletal muscle mitochondrial ATP production, protein synthesis, and mRNA transcripts. Proc. Natl. Acad. Sci U.S.A. 2003, 100:7996-8001.
37. Petersen K.F., et al. Decreased insulin-stimulated ATP synthesis and phosphate transport in muscle of insulin-resistant offspring of type 2 diabetic parents. PLoS Med. 2005, 2:e233.
38. Halvatsiotis P., et al. Synthesis rate of muscle proteins, muscle functions, and amino acid kinetics in type 2 diabetes. Diabetes 2002, 51:2395-2404.
39. Asmann Y.W., et al. Skeletal muscle mitochondrial functions, mitochondrial DNA copy numbers, and gene transcript profiles in type 2 diabetic and nondiabetic subjects at equal levels of low or high insulin and euglycemia. Diabetes 2006, 55:3309-3319.
40. Brown A.E., et al. Does impaired mitochondrial function affect insulin signaling and action in cultured human skeletal muscle cells?. Am. J. Physiol. Endocrinol. Metab. 2008, 294:E97-E102.
41. Nair K.S., et al. Asian Indians have enhanced skeletal muscle mitochondrial capacity to produce ATP in association with severe insulin resistance. Diabetes 2008, 57:1166-1175.
42. Toledo F.G., et al. Mitochondrial capacity in skeletal muscle is not stimulated by weight loss despite increases in insulin action and decreases in intramyocellular lipid content. Diabetes 2008, 57:987-994.
43. Schrauwen-Hinderling V.B., et al. The insulin-sensitizing effect of rosiglitazone in type 2 diabetes mellitus patients does not require improved in vivo muscle mitochondrial function. J. Clin. Endocrinol. Metab. 2008, 93:2917-2921.
44. Pagel-Langenickel I., et al. A discordance in rosiglitazone mediated insulin sensitization and skeletal muscle mitochondrial content/activity in type 2 diabetes mellitus. Am. J. Physiol. Heart Circ. Physiol. 2007, 293:H2659-H2666.
45. Brons C., et al. Mitochondrial function in skeletal muscle is normal and unrelated to insulin action in young men born with low birth weight. J. Clin. Endocrinol. Metab. 2008, 93:3885-3892.
46. Eriksen M.B., et al. Intact primary mitochondrial function in myotubes established from women with PCOS. J. Clin. Endocrinol. Metab. 2011, 96:E1298-E1302.
47. Gallagher I.J., et al. Integration of microRNA changes in vivo identifies novel molecular features of muscle insulin resistance in type 2 diabetes. Genome Med. 2010, 2:9.
48. Sleigh A., et al. Mitochondrial dysfunction in patients with primary congenital insulin resistance. J. Clin. Invest. 2011, 121:2457-2461.
49. Nielsen J., et al. 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. 2010, 298:E706-E713.
50. Phielix E., et al. Exercise training increases mitochondrial content and ex vivo mitochondrial function similarly in patients with type 2 diabetes and in control individuals. Diabetologia 2010, 53:1714-1721.
51. Hey-Mogensen M., et al. Effect of physical training on mitochondrial respiration and reactive oxygen species release in skeletal muscle in patients with obesity and type 2 diabetes. Diabetologia 2010, 53:1976-1985.
52. Heilbronn L.K., et al. Effect of 6-month calorie restriction on biomarkers of longevity, metabolic adaptation, and oxidative stress in overweight individuals: a randomized controlled trial. JAMA 2006, 295:1539-1548.
53. Larson-Meyer D.E., et al. Effect of calorie restriction with or without exercise on insulin sensitivity, beta-cell function, fat cell size, and ectopic lipid in overweight subjects. Diabetes Care 2006, 29:1337-1344.
54. Larson-Meyer D.E., et al. Effect of 6-month calorie restriction and exercise on serum and liver lipids and markers of liver function. Obesity (Silver Spring) 2008, 16:1355-1362.
55. Civitarese A.E., et al. Calorie restriction increases muscle mitochondrial biogenesis in healthy humans. PLoS Med. 2007, 4:e76.
56. Yamamoto H., et al. Sirtuin functions in health and disease. Mol. Endocrinol. 2007, 21:1745-1755.
57. de Kreutzenberg S.V., et al. Downregulation of the longevity-associated protein sirtuin 1 in insulin resistance and metabolic syndrome: potential biochemical mechanisms. Diabetes 2010, 59:1006-1015.
58. Rutanen J., et al. SIRT1 mRNA expression may be associated with energy expenditure and insulin sensitivity. Diabetes 2010, 59:829-835.
59. Frojdo S., et al. Phosphoinositide 3-kinase as a novel functional target for the regulation of the insulin signaling pathway by SIRT1. Mol. Cell. Endocrinol. 2011, 335:166-176.
60. Timmers S., et al. Calorie restriction-like effects of 30 days of resveratrol supplementation on energy metabolism and metabolic profile in obese humans. Cell Metab. 2011, 14:612-622.
61. Canto C., et al. AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity. Nature 2009, 458:1056-1060.