Role of mitochondrial function in insulin resistance

Advances in Experimental Medicine and Biology

Volumn 942, Issue , 2012, Pages 215-234

  Brands, Myrte ^a   Verhoeven, Arthur J ^a   Serlie, Mireille J ^a  

^a ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

Free fatty acids; Insulin resistance; Lipotoxicity; Mitochondrial function; Obesity; Oxidative phosphorylation

Indexed keywords

ADENOSINE TRIPHOSPHATE; CYTOCHROME C OXIDASE; FATTY ACID; INSULIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE (UBIQUINONE); UBIQUINOL CYTOCHROME C REDUCTASE;

ARTICLE; CAUSAL ATTRIBUTION; CELL FUNCTION; CELLULAR DISTRIBUTION; DISEASE ASSOCIATION; ENZYME ACTIVITY; ENZYME SYNTHESIS; EXTRACHROMOSOMAL INHERITANCE; GENE EXPRESSION REGULATION; HUMAN; INSULIN RESISTANCE; LIPID DIET; LIPOTOXICITY; MITOCHONDRIAL DNA DISORDER; MITOCHONDRIAL ENERGY TRANSFER; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; MITOCHONDRIAL VOLUME; MITOCHONDRIAL VOLUME DENSITY; MITOCHONDRION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OBESITY; OXIDATIVE PHOSPHORYLATION UNCOUPLING; OXYGEN CONSUMPTION; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RESPIRATORY CHAIN; SEDENTARY LIFESTYLE; SKELETAL MUSCLE; STRUCTURE ANALYSIS;

CASE-CONTROL STUDIES; HUMANS; INSULIN RESISTANCE; MEMBRANE POTENTIALS; MITOCHONDRIA; OBESITY;

EID: 84859881927     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-94-007-2869-1_9     Document Type: Article

References (107)

1. Andersen P, Saltin B (1985) Maximal perfusion of skeletal muscle in man. J Physiol 366:233-249
2. Asmann YW et al (2006) 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 55(12):3309-3319
3. Bach D et al (2003) Mitofusin-2 determines mitochondrial network architecture and mitochondrial metabolism. A novel regulatory mechanism altered in obesity. J Biol Chem 278(19):17190-17197
4. Bao S et al (1998) Expression of mRNAs encoding uncoupling proteins in human skeletal muscle: effects of obesity and diabetes. Diabetes 47(12):1935-1940
5. Baron AD et al (1993) Skeletal muscle blood flow. A possible link between insulin resistance and blood pressure. Hypertension 21(2):129-135
6. Befroy DE et al (2007) Impaired mitochondrial substrate oxidation in muscle of insulin-resistant offspring of type 2 diabetic patients. Diabetes 56(5):1376-1381
7. Belfort R et al (2005) Dose-response effect of elevated plasmafree fatty acid on insulin signaling. Diabetes 54(6):1640-1648
8. Berggren JR et al (2008) Skeletal muscle lipid oxidation and obesity: influence of weight loss and exercise. Am J Physiol Endocrinol Metab 294(4):E726-E732
9. Bergman RN (2007) Orchestration of glucose homeostasis: from asmall acorn to the Californiaoak. Diabetes 56(6):1489-1501
10. Boden G (2002) Interaction between free fatty acids and glucose metabolism. Curr Opin Clin Nutr Metab Care 5(5):545-549
11. Bonnard C et al (2008) Mitochondrial dysfunction results from oxidative stress in the skeletal muscle of diet-induced insulin-resistant mice. J Clin Invest 118(2):789-800
12. Boss O, Hagen T, Lowell BB (2000) Uncoupling proteins 2 and 3: potential regulators of mitochondrial energy metabolism. Diabetes 49(2):143-156
13. Bouchard C et al (1999) Familial aggregation of VO(2max) response to exercise training: results from the HERITAGE Family Study. J Appl Physiol 87(3):1003-1008
14. Boushel R et al (2007) Patients with type 2 diabetes have normal mitochondrial function in skeletal muscle. Diabetologia 50(4):790-796
15. Brands M et al (2011) Short-term increase of plasmafree fatty acids does not interfere with intrinsic mitochondrial function in healthy young men. Metabolism 60(10):1398-1405
16. Brehm A et al (2006) Increased lipid availability impairs insulin-stimulated ATP synthesis in human skeletal muscle. Diabetes 55(1):136-140
17. Brownlee M (2005) The pathobiology of diabetic complications: aunifying mechanism. Diabetes 54(6):1615-1625
18. Carter SL et al (2001) Changes in skeletal muscle in males and females following endurance training. Can J Physiol Pharmacol 79(5):386-392
19. Chavez AO et al (2010) Effect of short-term free Fatty acids elevation on mitochondrial function in skeletal muscle of healthy individuals. J Clin Endocrinol Metab 95(1):422-429
20. Chi MM et al (1983) Effects of detraining on enzymes of energy metabolism in individual human muscle fibers. Am J Physiol 244(3):C276-C287
21. Ciapaite J et al (2005) Modular kinetic analysis of the adenine nucleotide translocator-mediated effects of palmitoyl-CoA on the oxidative phosphorylation in isolated rat liver mitochondria. Diabetes 54(4):944-951
22. Civitarese AE, Ravussin E (2008) Mitochondrial energetics and insulin resistance. Endocrinology 149(3):950-954
23. Cogswell AM, Cogswell AM, Stevens RJ, Hood DA (1993) Properties of skeletal muscle mitochondriaisolated from subsarcolemmal and intermyofibrillar regions. Am J Physiol 264(2 Pt 1):C383-C389
24. Costford SR et al (2009) Increased susceptibility to oxidative damage in post-diabetic human myotubes. Diabetologia 52(11):2405-2415
25. De Feyter HM et al (2008) Early or advanced stage type 2 diabetes is not accompanied by in vivo skeletal muscle mitochondrial dysfunction. Eur J Endocrinol 158(5):643-653
26. DeFronzo RA et al (1985) Effects of insulin on peripheral and splanchnic glucose metabolism in noninsulin-dependent (type II) diabetes mellitus. J Clin Invest 76(1):149-155
27. Florez JC (2008) Newly identified loci highlight betacell dysfunction as akey cause of type 2 diabetes: where are the insulin resistance genes? Diabetologia51(7):1100-1110
28. Frayn KN (1983) Calculation of substrate oxidation rates in vivo from gaseous exchange. J Appl Physiol 55(2):628-634
29. Frederiksen CM et al (2008) Transcriptional profiling of myotubes from patients with type 2 diabetes: no evidence for aprimary defect in oxidative phosphorylation genes. Diabetologia51(11):2068-2077
30. Gadian DG, Radda GK (1981) NMR studies of tissue metabolism. Annu Rev Biochem 50:69-83
31. Gnaiger E (2009) Capacity of oxidative phosphorylation in human skeletal muscle. New perspectives of mitochondrial physiology. Int J Biochem Cell Biol 41(10):1837-1845
32. Guillet C et al (2009) Changes in basal and insulin and amino acid response of whole body and skeletal muscle proteins in obese men. J Clin Endocrinol Metab 94(8):3044-3050
33. Hancock CR et al (2008) High-fat diets cause insulin resistance despite an increase in muscle mitochondria. Proc Natl Acad Sci USA 105(22):7815-7820
34. He J, Watkins S, Kelley DE (2001) Skeletal muscle lipid content and oxidative enzyme activity in relation to muscle fiber type in type 2 diabetes and obesity. Diabetes 50(4):817-823
35. Heilbronn LK et al (2007) Markers of mitochondrial biogenesis and metabolism are lower in overweight and obese insulin-resistant subjects. J Clin Endocrinol Metab 92(4):1467-1473
36. Holloszy JO (2009) Skeletal muscle "mitochondrial deficiency" does not mediate insulin resistance. Am J Clin Nutr 89(1):463S-466S
37. Holloway GP, et al (2007) Skeletal muscle mitochondrial FAT/CD36 content and palmitate oxidation are not decreased in obese women. Am J Physiol Endocrinol Metab 292(6):E1782-E1789
38. Holloway GP, Bonen A, Spriet LL (2009) Regulation of skeletal muscle mitochondrial fatty acid metabolism in lean and obese individuals. Am J Clin Nutr 89(1):455S-462S
39. Hood DA (2001) Invited Review: contractile activity-induced mitochondrial biogenesis in skeletal muscle. J Appl Physiol 90(3):1137-1157
40. Hoppeler H et al (1985) Endurance training in humans: aerobic capacity and structure of skeletal muscle. J Appl Physiol 59(2):320-327
41. Karakelides H et al (2010) Age, obesity, and sex effects on insulin sensitivity and skeletal muscle mitochondrial function. Diabetes 59(1):89-97
42. Kelley DE et al (2002) Dysfunction of mitochondriain human skeletal muscle in type 2 diabetes. Diabetes 51(10):2944-2950
43. Kemp GJ, Taylor DJ, Radda GK (1993) Control of phosphocreatine resynthesis during recovery from exercise in human skeletal muscle. NMR Biomed 6(1):66-72
44. Khalfallah Y et al (2000) Regulation of uncoupling protein-2 and uncoupling protein-3 mRNA expression during lipid infusion in human skeletal muscle and subcutaneous adipose tissue. Diabetes 49(1):25-31
45. Koutsari C, Jensen MD (2006) Thematic review series: patient-oriented research. Free fatty acid metabolism in human obesity. J Lipid Res 47(8):1643-1650
46. Koves TR et al (2005) Subsarcolemmal and intermyofibrillar mitochondriaplay distinct roles in regulating skeletal muscle fatty acid metabolism. Am J Physiol Cell Physiol 288(5):C1074-C1082
47. Koves TR et al (2008) Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance. Cell Metab 7(1):45-56
48. Krook A et al (1998) Uncoupling protein 3 is reduced in skeletal muscle of NIDDM patients. Diabetes 47(9):1528-1531
49. Larsson L, Ansved T (1985) Effects of long-term physical training and detraining on enzyme histochemical and functional skeletal muscle characteristic in man. Muscle Nerve 8(8):714-722
50. Malenfant P et al (2001) Fat content in individual muscle fibers of lean and obese subjects. Int J Obes Relat Metab Disord 25(9):1316-1321
51. Meex RC et al (2010) 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(3):572-579
52. Menshikova EV et al (2005) Effects of weight loss and physical activity on skeletal muscle mitochondrial function in obesity. Am J Physiol Endocrinol Metab 288(4):E818-E825
53. Menshikova EV et al (2006) Effects of exercise on mitochondrial content and function in aging human skeletal muscle. J Gerontol A Biol Sci Med Sci 61(6):534-540
54. Mogensen M et al (2007) Mitochondrial respiration is decreased in skeletal muscle of patients with type 2 diabetes. Diabetes 56(6):1592-1599
55. Mootha VK et al (2003) PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 34(3):267-273
56. Morino K et al (2005) Reduced mitochondrial density and increased IRS-1 serine phosphorylation in muscle of insulinresistant offspring of type 2 diabetic parents. J Clin Invest 115(12):3587-3593
57. Nair KS et al (2008) Asian Indians have enhanced skeletal muscle mitochondrial capacity to produce ATP in association with severe insulin resistance. Diabetes 57(5):1166-1175
58. Nuutila P et al (2000) Enhanced stimulation of glucose uptake by insulin increases exercise-stimulated glucose uptake in skeletal muscle in humans: studies using [15O]O2, [15O]H2O, [18F]fluoro-deoxy-glucose, and positron emission tomography. Diabetes 49(7):1084-1091
59. Nyholm B et al (1997) Evidence of an increased number of type IIb muscle fibers in insulin-resistant first-degree relatives of patients with NIDDM. Diabetes 46(11):1822-1828
60. Oberbach A et al (2006) Altered fiber distribution and fiber-specific glycolytic and oxidative enzyme activity in skeletal muscle of patients with type 2 diabetes. Diabetes Care 29(4):895-900
61. Ogata T, Yamasaki Y (1997) Ultra-high-resolution scanning electron microscopy of mitochondriaand sarcoplasmic reticulum arrangement in human red, white, and intermediate muscle fibers. Anat Rec 248(2):214-223
62. Patti ME et al (2003) Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: potential role of PGC1 and NRF1. Proc Natl Acad Sci USA 100(14):8466-8471
63. Perseghin G et al (1997) Metabolic defects in lean nondiabetic offspring of NIDDM parents: across-sectional study. Diabetes 46(6):1001-1009
64. Petersen KF et al (2004) Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N Engl J Med 350(7):664-671
65. Pette D, Staron RS (1997) Mammalian skeletal muscle fiber type transitions. Int Rev Cytol 170:143-223
66. Phielix E et al (2008) Lower intrinsic ADP-stimulated mitochondrial respiration underlies in vivo mitochondrial dysfunction in muscle of male type 2 diabetic patients. Diabetes 57(11):2943-2949
67. Pilegaard H, Saltin B, Neufer PD (2003) Exercise induces transient transcriptional activation of the PGC-1alphagene in human skeletal muscle. J Physiol 546(Pt 3):851-858
68. Puntschart A et al (1995) mRNAs of enzymes involved in energy metabolism and mtDNA are increased in endurancetrained athletes. Am J Physiol 269(3 Pt 1):C619-C625
69. Rabol R et al (2010) Regional anatomic differences in skeletal muscle mitochondrial respiration in type 2 diabetes and obesity. J Clin Endocrinol Metab 95(2):857-863
70. Rasmussen UF, Rasmussen HN (2000a) Human quadriceps muscle mitochondria: afunctional characterization. Mol Cell Biochem 208(1-2):37-44
71. Rasmussen UF, Rasmussen HN (2000b) Human skeletal muscle mitochondrial capacity. ActaPhysiol Scand 168(4):473-480
72. Richardson DK et al (2005) Lipid infusion decreases the expression of nuclear encoded mitochondrial genes and increases the expression of extracellular matrix genes in human skeletal muscle. J Biol Chem 280(11):10290-10297
73. Ritov VB, Menshikova EV, Kelley DE (2004) High-performance liquid chromatography-based methods of enzymatic analysis: electron transport chain activity in mitochondriafrom human skeletal muscle. Anal Biochem 333(1):27-38
74. Ritov VB et al (2005) Deficiency of subsarcolemmal mitochondriain obesity and type 2 diabetes. Diabetes 54(1):8-14
75. Ritov VB, Menshikova EV, Kelley DE (2006) Analysis of cardiolipin in human muscle biopsy. J Chromatogr B Analyt Technol Biomed Life Sci 831(1-2):63-71
76. Roden M (2005) Muscle triglycerides and mitochondrial function: possible mechanisms for the development of type 2 diabetes. Int J Obes (Lond) 29(S111)
77. Rolfe DF, Brand MD (1996) Contribution of mitochondrial proton leak to skeletal muscle respiration and to standard metabolic rate. Am J Physiol 271(4 Pt 1):C1380-C1389
78. Russell AP et al (2003) Lipid peroxidation in skeletal muscle of obese as compared to endurance-trained humans: acase of good vs. bad lipids? FEBS Lett 551(1-3):104-106
79. Sahlin K, Sahlin K et al (1997) Phosphocreatine content in single fibers of human muscle after sustained submaximal exercise. Am J Physiol 273(1 Pt 1):C172-C178
80. Scaduto RC Jr, Grotyohann LW (1999) Measurement of mitochondrial membrane potential using fluorescent rhodamine derivatives. Biophys J 76(1 Pt 1):469-477
81. Schrauwen P (2007) High-fat diet, muscular lipotoxicity and insulin resistance. Proc Nutr Soc 66(1):33-41
82. Schrauwen P, Hesselink MK (2004) Oxidative capacity, lipotoxicity, and mitochondrial damage in type 2 diabetes. Diabetes 53(6):1412-1417
83. Schrauwen-Hinderling VB et al (2007) Impaired in vivo mitochondrial function but similar intramyocellular lipid content in patients with type 2 diabetes mellitus and BMI-matched control subjects. Diabetologia50(1):113-120
84. Shoffner JM, Wallace DC (1992) Mitochondrial genetics: principles and practice. Am J Hum Genet 51(6): 1179-1186
85. Short KR et al (2005) Decline in skeletal muscle mitochondrial function with aging in humans. Proc Natl Acad Sci USA 102(15):5618-5623
86. Shulman GI (2000) Cellular mechanisms of insulin resistance. J Clin Invest 106(2):171-176
87. Shulman RG, Rothman DL (2001) 13C NMR of intermediary metabolism: implications for systemic physiology. Annu Rev Physiol 63:15-48
88. Simoneau JA, Bouchard C (1989) Human variation in skeletal muscle fiber-type proportion and enzyme activities. Am J Physiol 257(4 Pt 1):E567-E572
89. Sreekumar R et al (2002) Gene expression profile in skeletal muscle of type 2 diabetes and the effect of insulin treatment. Diabetes 51(6):1913-1920
90. Stump CS et al (2003) Effect of insulin on human skeletal muscle mitochondrial ATP production, protein synthesis, and mRNA transcripts. Proc Natl Acad Sci USA 100(13):7996-8001
91. Szendroedi J, Roden M (2008) Mitochondrial fitness and insulin sensitivity in humans. Diabetologia 51(12):2155-2167
92. Szendroedi J et al (2007) Muscle mitochondrial ATP synthesis and glucose transport/phosphorylation in type 2 diabetes. PLoS Med 4(5):e154
93. Tanner CJ et al (2002) Muscle fiber type is associated with obesity and weight loss. Am J Physiol Endocrinol Metab 282(6):E1191-E1196
94. Tarnopolsky MA et al (2007) 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(3):R1271-R1278
95. Thamer C et al (2003) Reduced skeletal muscle oxygen uptake and reduced beta-cell function: two early abnormalities in normal glucose-tolerant offspring of patients with type 2 diabetes. Diabetes Care 26(7):2126-2132
96. Toledo FG, Watkins S, Kelley DE (2006) Changes induced by physical activity and weight loss in the morphology of intermyofibrillar mitochondriain obese men and women. J Clin Endocrinol Metab 91(8):3224-3227
97. Toledo FG et al (2008) Mitochondrial capacity in skeletal muscle is not stimulated by weight loss despite increases in insulin action and decreases in intramyocellular lipid content. Diabetes 57(4):987-994
98. Tonkonogi M, Sahlin K (1997) Rate of oxidative phosphorylation in isolated mitochondriafrom human skeletal muscle: effect of training status. ActaPhysiol Scand 161(3):345-353
99. Tonkonogi M, Harris B, Sahlin K (1997) Increased activity of citrate synthase in human skeletal muscle after asingle bout of prolonged exercise. ActaPhysiol Scand 161(3):435-436
100. Twig G, Hyde B, Shirihai OS (2008) Mitochondrial fusion, fission and autophagy as aquality control axis: the bioenergetic view. Biochim Biophys Acta 1777(9):1092-1097
101. Ukropcova B et al (2007) Family history of diabetes links impaired substrate switching and reduced mitochondrial content in skeletal muscle. Diabetes 56(3):720-727
102. van den Broek NM et al (2010) Increased mitochondrial content rescues in vivo muscle oxidative capacity in long-term high-fat-diet-fed rats. FASEB J 24(5):1354-1364
103. Vondra K et al (1977) Enzyme activities in quadriceps femoris muscle of obese diabetic male patients. Diabetologia 13(5):527-529
104. Wang H et al (1999) Relationships between muscle mitochondrial DNA content, mitochondrial enzyme activity and oxidative capacity in man: alterations with disease. Eur J Appl Physiol Occup Physiol 80(1):22-27
105. Wibom R, Hagenfeldt L, von Dobeln U (2002) Measurement of ATP production and respiratory chain enzyme activities in mitochondriaisolated from small muscle biopsy samples. Anal Biochem 311(2):139-151
106. Wittig I, Schagger H (2009) Supramolecular organization of ATP synthase and respiratory chain in mitochondrial membranes. Biochim Biophys Acta 1787(6):672-680
107. Wu Z et al (1999) Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98(1):115-124