Mitochondrial function in metabolic health: A genetic and environmental tug of war

Biochimica et Biophysica Acta - General Subjects

Volumn 1840, Issue 4, 2014, Pages 1285-1294

  Stephenson, Erin J ^a   Hawley, John A ^b,c  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^b AUSTRALIAN CATHOLIC UNIVERSITY   (Australia)

^c LIVERPOOL JOHN MOORES UNIVERSITY   (United Kingdom)

Author keywords

Exercise; Inactivity; Metabolic health; Metabolism; Mitochondria; Skeletal muscle

Indexed keywords

TRICARBOXYLIC ACID;

ARTICLE; CARBOHYDRATE METABOLISM; CITRIC ACID CYCLE; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENVIRONMENTAL FACTOR; EXERCISE; FATTY ACID METABOLISM; GENE STRUCTURE; GENETIC ASSOCIATION; GENETIC SUSCEPTIBILITY; GENOTYPE ENVIRONMENT INTERACTION; HUMAN; INSULIN RESISTANCE; LIPID OXIDATION; METABOLIC DISORDER; MITOCHONDRIAL RESPIRATION; MUSCLE FUNCTION; NONHUMAN; PHYSICAL ACTIVITY; PRIORITY JOURNAL; SKELETAL MUSCLE;

EXERCISE; INACTIVITY; METABOLIC HEALTH; METABOLISM; MITOCHONDRIA; SKELETAL MUSCLE;

ANIMALS; EXERCISE; GENE-ENVIRONMENT INTERACTION; HUMANS; METABOLIC DISEASES; MITOCHONDRIA; PHYSICAL FITNESS; SEDENTARY LIFESTYLE;

EID: 84895539245     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2013.12.004     Document Type: Article

References (151)

1. J.R. Zierath, and J.A. Hawley Skeletal muscle fiber type: influence on contractile and metabolic properties PLoS Biol. 2 2004 e348
2. F.W. Booth, and D.B. Thomason Molecular and cellular adaptation of muscle in response to exercise: perspectives of various models Physiol. Rev. 71 1991 541 585
3. M. Fluck, and H. Hoppeler Molecular basis of skeletal muscle plasticity - from gene to form and function Rev. Physiol. Biochem. Pharmacol. 146 2003 159 216
4. S. Schiaffino, and C. Reggiani Molecular diversity of myofibrillar proteins: gene regulation and functional significance Physiol. Rev. 76 1996 371 423
5. R.A. DeFronzo, R. Gunnarsson, O. Bjorkman, M. Olsson, and J. Wahren Effects of insulin on peripheral and splanchnic glucose metabolism in noninsulin-dependent (type II) diabetes mellitus J. Clin. Invest. 76 1985 149 155
6. H.J. Woerle, C. Meyer, J.M. Dostou, N.R. Gosmanov, N. Islam, E. Popa, S.D. Wittlin, S.L. Welle, and J.E. Gerich Pathways for glucose disposal after meal ingestion in humans Am. J. Physiol. Endocrinol. Metab. 284 2003 E716 E725
7. C. Meyer, H.J. Woerle, J.M. Dostou, S.L. Welle, and J.E. Gerich Abnormal renal, hepatic, and muscle glucose metabolism following glucose ingestion in type 2 diabetes Am. J. Physiol. Endocrinol. Metab. 287 2004 E1049 E1056
8. D.E. Kelley, J. He, E.V. Menshikova, and V.B. Ritov Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes Diabetes 51 2002 2944 2950
9. V.B. Ritov, E.V. Menshikova, K. Azuma, R. Wood, F.G. Toledo, B.H. Goodpaster, N.B. Ruderman, and D.E. Kelley Deficiency of electron transport chain in human skeletal muscle mitochondria in type 2 diabetes mellitus and obesity Am. J. Physiol. Endocrinol. Metab. 298 2010 E49 E58
10. J.A. Hawley, and J.O. Holloszy Exercise: it's the real thing! Nutr. Rev. 67 2009 172 178
11. P. Poulsen, A. Vaag, K. Kyvik, and H. Beck-Nielsen Genetic versus environmental aetiology of the metabolic syndrome among male and female twins Diabetologia 44 2001 537 543
12. H.M. Roche, C. Phillips, and M.J. Gibney The metabolic syndrome: the crossroads of diet and genetics Proc. Nutr. Soc. 64 2005 371 377
13. J.C. Wells, and M. Siervo Obesity and energy balance: is the tail wagging the dog? Eur. J. Clin. Nutr. 65 2011 1173 1189
14. J.A. Hawley Exercise as a therapeutic intervention for the prevention and treatment of insulin resistance Diabetes Metab. Res. Rev. 20 2004 383 393
15. T.J. Saunders, R. Larouche, R.C. Colley, and M.S. Tremblay Acute sedentary behaviour and markers of cardiometabolic risk: a systematic review of intervention studies J. Nutr. Metab. 2012 2012 712435
16. F.W. Booth, M.V. Chakravarthy, and E.E. Spangenburg Exercise and gene expression: physiological regulation of the human genome through physical activity J. Physiol. 543 2002 399 411
17. F. Lindgarde, and B. Saltin Daily physical activity, work capacity and glucose tolerance in lean and obese normoglycaemic middle-aged men Diabetologia 20 1981 134 138
18. J. Cederholm, and L. Wibell Glucose tolerance and physical activity in a health survey of middle-aged subjects Acta Med. Scand. 217 1985 373 378
19. J.T. Wang, L.T. Ho, K.T. Tang, L.M. Wang, Y.D. Chen, and G.M. Reaven Effect of habitual physical activity on age-related glucose intolerance J. Am. Geriatr. Soc. 37 1989 203 209
20. A.M. Kriska, R.E. LaPorte, D.J. Pettitt, M.A. Charles, R.G. Nelson, L.H. Kuller, P.H. Bennett, and W.C. Knowler The association of physical activity with obesity, fat distribution and glucose intolerance in Pima Indians Diabetologia 36 1993 863 869
21. M.A. Pereira, A.M. Kriska, M.L. Joswiak, G.K. Dowse, V.R. Collins, P.Z. Zimmet, H. Gareeboo, P. Chitson, F. Hemraj, A. Purran, and D. Fareed Physical inactivity and glucose-intolerance in the multiethnic island of Mauritius Med. Sci. Sports Exerc. 27 1995 1626 1634
22. J.G. Regensteiner, S.M. Shetterly, E.J. Mayer, R.H. Eckel, W.L. Haskell, J. Baxter, and R.F. Hamman Relationship between habitual physical activity and insulin area among individuals with impaired glucose tolerance. The San Luis Valley Diabetes Study Diabetes Care 18 1995 490 497
23. V.K. Mootha, C.M. Lindgren, K.F. Eriksson, A. Subramanian, S. Sihag, J. Lehar, P. Puigserver, E. Carlsson, M. Ridderstrale, E. Laurila, N. Houstis, M.J. Daly, N. Patterson, J.P. Mesirov, T.R. Golub, P. Tamayo, B. Spiegelman, E.S. Lander, J.N. Hirschhorn, D. Altshuler, and L.C. Groop PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes Nat. Genet. 34 2003 267 273
24. M.E. Patti, A.J. Butte, S. Crunkhorn, K. Cusi, R. Berria, S. Kashyap, Y. Miyazaki, I. Kohane, M. Costello, R. Saccone, E.J. Landaker, A.B. Goldfine, E. Mun, R. DeFronzo, J. Finlayson, C.R. Kahn, and L.J. Mandarino 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. 100 2003 8466 8471
25. M. Wei, J.B. Kampert, C.E. Barlow, M.Z. Nichaman, L.W. Gibbons, R.S. Paffenbarger Jr., and S.N. Blair Relationship between low cardiorespiratory fitness and mortality in normal-weight, overweight, and obese men JAMA 282 1999 1547 1553
26. J. Myers, M. Prakash, V. Froelicher, D. Do, S. Partington, and J.E. Atwood Exercise capacity and mortality among men referred for exercise testing N. Engl. J. Med. 346 2002 793 801
27. J.A. Hawley, and S.J. Lessard Exercise training-induced improvements in insulin action Acta Physiol. 192 2008 127 135
28. S.R. Colberg, A.L. Albright, B.J. Blissmer, B. Braun, L. Chasan-Taber, B. Fernhall, J.G. Regensteiner, R.R. Rubin, R.J. Sigal, M. American College of Sports, and A. American Diabetes Exercise and type 2 diabetes: American College of Sports Medicine and the American Diabetes Association: joint position statement. Exercise and type 2 diabetes Med. Sci. Sports Exerc. 42 2010 2282 2303
29. M. Rosenthal, W.L. Haskell, R. Solomon, A. Widstrom, and G.M. Reaven Demonstration of a relationship between level of physical training and insulin-stimulated glucose utilization in normal humans Diabetes 32 1983 408 411
30. J.O. Clausen, K. Borch-Johnsen, H. Ibsen, R.N. Bergman, P. Hougaard, K. Winther, and O. Pedersen Insulin sensitivity index, acute insulin response, and glucose effectiveness in a population-based sample of 380 young healthy Caucasians. Analysis of the impact of gender, body fat, physical fitness, and life-style factors J. Clin. Invest. 98 1996 1195 1209
31. S.W. Farrell, C.E. Finley, and S.M. Grundy Cardiorespiratory fitness, LDL cholesterol, and CHD mortality in men Med. Sci. Sports Exerc. 44 2012 2132 2137
32. L.G. Koch, and S.L. Britton Divergent selection for aerobic capacity in rats as a model for complex disease Integr. Comp. Biol. 45 2005 405 415
33. B. Saltin Hemodynamic adaptations to exercise Am. J. Cardiol. 55 1985 42D 47D
34. 2 consumption in man after prolonged bed rest J. Physiol. 501 Pt 3 1997 677 686
35. M. Burtscher Exercise limitations by the oxygen delivery and utilization systems in aging and disease: coordinated adaptation and deadaptation of the lung-heart muscle axis - a mini-review Gerontology 59 2012 289 296
36. R.A. Jacobs, P. Rasmussen, C. Siebenmann, V. Diaz, M. Gassmann, D. Pesta, E. Gnaiger, N.B. Nordsborg, P. Robach, and C. Lundby Determinants of time trial performance and maximal incremental exercise in highly trained endurance athletes J. Appl. Physiol. 111 2011 1422 1430
37. R.A. Jacobs, and C. Lundby Mitochondria express enhanced quality as well as quantity in association with aerobic fitness across recreationally active individuals up to elite athletes J. Appl. Physiol. 114 2013 344 350
38. P.M. Coen, S.A. Jubrias, G. Distefano, F. Amati, D.C. Mackey, N.W. Glynn, T.M. Manini, S.E. Wohlgemuth, C. Leeuwenburgh, S.R. Cummings, A.B. Newman, L. Ferrucci, F.G. Toledo, E. Shankland, K.E. Conley, and B.H. Goodpaster Skeletal muscle mitochondrial energetics are associated with maximal aerobic capacity and walking speed in older adults J. Gerontol. A Biol. Sci. Med. Sci. 68 2013 447 455
39. A.M. Jones, and H. Carter The effect of endurance training on parameters of aerobic fitness Sports Med. 29 2000 373 386
40. B.F. Hurley, J.M. Hagberg, W.K. Allen, D.R. Seals, J.C. Young, R.W. Cuddihee, and J.O. Holloszy Effect of training on blood lactate levels during submaximal exercise J. Appl. Physiol. 56 1984 1260 1264
41. R. Ramsbottom, C. Williams, N. Fleming, and M.L. Nute Training induced physiological and metabolic changes associated with improvements in running performance Br. J. Sports Med. 23 1989 171 176
42. M. Tonkonogi, and K. Sahlin Rate of oxidative phosphorylation in isolated mitochondria from human skeletal muscle: effect of training status Acta Physiol. Scand. 161 1997 345 353
43. D.E. Kelley, M. Mokan, J.A. Simoneau, and L.J. Mandarino Interaction between glucose and free fatty acid metabolism in human skeletal muscle J. Clin. Invest. 92 1993 91 98
44. D.E. Kelley Skeletal muscle triglycerides: an aspect of regional adiposity and insulin resistance Ann. N. Y. Acad. Sci. 967 2002 135 145
45. H.A. Krebs The citric acid cycle and the Szent-Gyorgyi cycle in pigeon breast muscle Biochem. J. 34 1940 775 779
46. P.B. Garland, D. Shepherd, D.G. Nicholls, D.W. Yates, and P.A. Light Interactions between fatty acid oxidation and the tricarboxylic acid cycle J.M. Lowenstein, Citric Acid Cycle: Control and Compartmentation, Dekker 1969 163 212
47. P. Mitchell Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism Nature 191 1961 144 148
48. B. Saltin, and P.D. Gollnick Skeletal muscle adaptability: significance for metabolism and performance Handbook of Physiology. Skeletal Muscle 1983 Am Physiol Soc Bethesda, MD 555 632
49. J.O. Holloszy Biochemical adaptations in muscle. Effects of exercise on mitochondrial oxygen uptake and respiratory enzyme activity in skeletal muscle J. Biol. Chem. 242 1967 2278 2282
50. P.A. Mole, L.B. Oscai, and J.O. Holloszy Adaptation of muscle to exercise. Increase in levels of palmityl Coa synthetase, carnitine palmityltransferase, and palmityl Coa dehydrogenase, and in the capacity to oxidize fatty acids J. Clin. Invest. 50 1971 2323 2330
51. J.O. Holloszy, and E.F. Coyle Adaptations of skeletal muscle to endurance exercise and their metabolic consequences J. Appl. Physiol. 56 1984 831 838
52. B. Korzeniewski, and J.A. Zoladz Training-induced adaptation of oxidative phosphorylation in skeletal muscles Biochem. J. 374 2003 37 40
53. M.J. Joyner, and E.F. Coyle Endurance exercise performance: the physiology of champions J. Physiol. 586 2008 35 44
54. H. Pilegaard, B. Saltin, and P.D. Neufer Exercise induces transient transcriptional activation of the PGC-1alpha gene in human skeletal muscle J. Physiol. 546 2003 851 858
55. A.P. Russell, M.K. Hesselink, S.K. Lo, and P. Schrauwen Regulation of metabolic transcriptional co-activators and transcription factors with acute exercise FASEB J. 19 2005 986 988
56. K.S. Rockl, C.A. Witczak, and L.J. Goodyear Signaling mechanisms in skeletal muscle: acute responses and chronic adaptations to exercise IUBMB Life 60 2008 145 153
57. M.J. Gibala, S.L. McGee, A.P. Garnham, K.F. Howlett, R.J. Snow, and M. Hargreaves Brief intense interval exercise activates AMPK and p38 MAPK signaling and increases the expression of PGC-1alpha in human skeletal muscle J. Appl. Physiol. 106 2009 929 934
58. D.A. Hood Mechanisms of exercise-induced mitochondrial biogenesis in skeletal muscle Appl. Physiol. Nutr. Metab. 34 2009 465 472
59. J.P. Little, A. Safdar, D. Bishop, M.A. Tarnopolsky, and M.J. Gibala An acute bout of high-intensity interval training increases the nuclear abundance of PGC-1alpha and activates mitochondrial biogenesis in human skeletal muscle Am. J. Physiol. Regul. Integr. Comp. Physiol. 300 2011 R1303 R1310
60. A. Safdar, J.P. Little, A.J. Stokl, B.P. Hettinga, M. Akhtar, and M.A. Tarnopolsky Exercise increases mitochondrial PGC-1alpha content and promotes nuclear-mitochondrial cross-talk to coordinate mitochondrial biogenesis J. Biol. Chem. 286 2011 10605 10617
61. J.D. Bartlett, C. Hwa Joo, T.S. Jeong, J. Louhelainen, A.J. Cochran, M.J. Gibala, W. Gregson, G.L. Close, B. Drust, and J.P. Morton Matched work high-intensity interval and continuous running induce similar increases in PGC-1alpha mRNA, AMPK, p38, and p53 phosphorylation in human skeletal muscle J. Appl. Physiol. 112 2012 1135 1143
62. W.K. Yeo, A.L. Carey, L. Burke, L.L. Spriet, and J.A. Hawley Fat adaptation in well-trained athletes: effects on cell metabolism Appl. Physiol. Nutr. Metab. 36 2011 12 22
63. Y. Manabe, K.S. Gollisch, L. Holton, Y.B. Kim, J. Brandauer, N.L. Fujii, M.F. Hirshman, and L.J. Goodyear Exercise training-induced adaptations associated with increases in skeletal muscle glycogen content FEBS J. 280 2013 916 926
64. C.G. Perry, J. Lally, G.P. Holloway, G.J. Heigenhauser, A. Bonen, and L.L. Spriet Repeated transient mRNA bursts precede increases in transcriptional and mitochondrial proteins during training in human skeletal muscle J. Physiol. 588 2010 4795 4810
65. B.B. Lowell, and G.I. Shulman Mitochondrial dysfunction and type 2 diabetes Science 307 2005 384 387
66. I. Dahlman, M. Forsgren, A. Sjogren, E.A. Nordstrom, M. Kaaman, E. Naslund, A. Attersand, and P. Arner Downregulation of electron transport chain genes in visceral adipose tissue in type 2 diabetes independent of obesity and possibly involving tumor necrosis factor-alpha Diabetes 55 2006 1792 1799
67. M. Wang, X.C. Wang, Z.Y. Zhang, B. Mou, and R.M. Hu Impaired mitochondrial oxidative phosphorylation in multiple insulin-sensitive tissues of humans with type 2 diabetes mellitus J. Int. Med. Res. 38 2010 769 781
68. L.M. Sparks, H. Xie, R.A. Koza, R. Mynatt, M.W. Hulver, G.A. Bray, and S.R. Smith A high-fat diet coordinately downregulates genes required for mitochondrial oxidative phosphorylation in skeletal muscle Diabetes 54 2005 1926 1933
69. S. Crunkhorn, F. Dearie, C. Mantzoros, H. Gami, W.S. da Silva, D. Espinoza, R. Faucette, K. Barry, A.C. Bianco, and M.E. Patti Peroxisome proliferator activator receptor gamma coactivator-1 expression is reduced in obesity: potential pathogenic role of saturated fatty acids and p38 mitogen-activated protein kinase activation J. Biol. Chem. 282 2007 15439 15450
70. J.X. Rong, Y. Qiu, M.K. Hansen, L. Zhu, V. Zhang, M. Xie, Y. Okamoto, M.D. Mattie, H. Higashiyama, S. Asano, J.C. Strum, and T.E. Ryan Adipose mitochondrial biogenesis is suppressed in db/db and high-fat diet-fed mice and improved by rosiglitazone Diabetes 56 2007 1751 1760
71. L.N. Sutherland, L.C. Capozzi, N.J. Turchinsky, R.C. Bell, and D.C. Wright Time course of high-fat diet-induced reductions in adipose tissue mitochondrial proteins: potential mechanisms and the relationship to glucose intolerance Am. J. Physiol. Endocrinol. Metab. 295 2008 E1076 E1083
72. M.J. Laye, R.S. Rector, S.O. Warner, S.P. Naples, A.L. Perretta, G.M. Uptergrove, M.H. Laughlin, J.P. Thyfault, F.W. Booth, and J.A. Ibdah Changes in visceral adipose tissue mitochondrial content with type 2 diabetes and daily voluntary wheel running in OLETF rats J. Physiol. 587 2009 3729 3739
73. J.O. Holloszy Skeletal muscle "mitochondrial deficiency" does not mediate insulin resistance Am. J. Clin. Nutr. 89 2009 463S 466S
74. J.O. Holloszy "Deficiency" of mitochondria in muscle does not cause insulin resistance Diabetes 62 2013 1036 1040
75. B.H. Goodpaster Mitochondrial deficiency is associated with insulin resistance Diabetes 62 2013 1032 1035
76. L. Storlien, N.D. Oakes, and D.E. Kelley Metabolic flexibility Proc. Nutr. Soc. 63 2004 363 368
77. D.E. Kelley, and J.A. Simoneau Impaired free fatty acid utilization by skeletal muscle in non-insulin-dependent diabetes mellitus J. Clin. Invest. 94 1994 2349 2356
78. D.E. Kelley, B. Goodpaster, R.R. Wing, and J.A. Simoneau Skeletal muscle fatty acid metabolism in association with insulin resistance, obesity, and weight loss Am. J. Physiol. 277 1999 E1130 E1141
79. J.D. McGarry Banting lecture 2001: dysregulation of fatty acid metabolism in the etiology of type 2 diabetes Diabetes 51 2002 7 18
80. J.A. Simoneau, J.H. Veerkamp, L.P. Turcotte, and D.E. Kelley Markers of capacity to utilize fatty acids in human skeletal muscle: relation to insulin resistance and obesity and effects of weight loss FASEB J. 13 1999 2051 2060
81. G. De Pergola, N. Pannacciulli, A. Minenna, R.A. Martina, F. Cannito, and R. Giorgino Fuel metabolism in adult individuals with a wide range of body mass index: effect of a family history of type 2 diabetes Diabetes Nutr. Metab. 16 2003 41 47
82. G. Lattuada, F. Costantino, A. Caumo, P. Scifo, F. Ragogna, F. De Cobelli, A. Del Maschio, L. Luzi, and G. Perseghin Reduced whole-body lipid oxidation is associated with insulin resistance, but not with intramyocellular lipid content in offspring of type 2 diabetic patients Diabetologia 48 2005 741 747
83. J.Y. Kim, R.C. Hickner, R.L. Cortright, G.L. Dohm, and J.A. Houmard Lipid oxidation is reduced in obese human skeletal muscle Am. J. Physiol. Endocrinol. Metab. 279 2000 E1039 E1044
84. M.W. Hulver, J.R. Berggren, R.N. Cortright, R.W. Dudek, R.P. Thompson, W.J. Pories, K.G. MacDonald, G.W. Cline, G.I. Shulman, G.L. Dohm, and J.A. Houmard Skeletal muscle lipid metabolism with obesity Am. J. Physiol. Endocrinol. Metab. 284 2003 E741 E747
85. K.E. Boyle, D. Zheng, E.J. Anderson, P.D. Neufer, and J.A. Houmard Mitochondrial lipid oxidation is impaired in cultured myotubes from obese humans Int. J. Obes. 36 2012 1025 1031
86. G.M. Battaglia, D. Zheng, R.C. Hickner, and J.A. Houmard Effect of exercise training on metabolic flexibility in response to a high-fat diet in obese individuals Am. J. Physiol. Endocrinol. Metab. 303 2012 E1440 E1445
87. C. Bonnard, A. Durand, S. Peyrol, E. Chanseaume, M.A. Chauvin, B. Morio, H. Vidal, and J. Rieusset Mitochondrial dysfunction results from oxidative stress in the skeletal muscle of diet-induced insulin-resistant mice J. Clin. Invest. 118 2008 789 800
88. R.C. Noland, T.R. Koves, S.E. Seiler, H. Lum, R.M. Lust, O. Ilkayeva, R.D. Stevens, F.G. Hegardt, and D.M. Muoio Carnitine insufficiency caused by aging and overnutrition compromises mitochondrial performance and metabolic control J. Biol. Chem. 284 2009 22840 22852
89. V.B. Ritov, E.V. Menshikova, J. He, R.E. Ferrell, B.H. Goodpaster, and D.E. Kelley Deficiency of subsarcolemmal mitochondria in obesity and type 2 diabetes Diabetes 54 2005 8 14
90. C. Guillet, I. Delcourt, M. Rance, C. Giraudet, S. Walrand, M. Bedu, P. Duche, and Y. Boirie Changes in basal and insulin and amino acid response of whole body and skeletal muscle proteins in obese men J. Clin. Endocrinol. Metab. 94 2009 3044 3050
91. T.R. Koves, J.R. Ussher, R.C. Noland, D. Slentz, M. Mosedale, O. Ilkayeva, J. Bain, R. Stevens, J.R. Dyck, C.B. Newgard, G.D. Lopaschuk, and D.M. Muoio Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance Cell Metab. 7 2008 45 56
92. E. Phielix, V.B. Schrauwen-Hinderling, M. Mensink, E. Lenaers, R. Meex, J. Hoeks, M.E. Kooi, E. Moonen-Kornips, J.P. Sels, M.K. Hesselink, and P. Schrauwen Lower intrinsic ADP-stimulated mitochondrial respiration underlies in vivo mitochondrial dysfunction in muscle of male type 2 diabetic patients Diabetes 57 2008 2943 2949
93. M.A. Abdul-Ghani, F.L. Muller, Y. Liu, A.O. Chavez, B. Balas, P. Zuo, Z. Chang, D. Tripathy, R. Jani, M. Molina-Carrion, A. Monroy, F. Folli, H. Van Remmen, and R.A. DeFronzo Deleterious action of FA metabolites on ATP synthesis: possible link between lipotoxicity, mitochondrial dysfunction, and insulin resistance Am. J. Physiol. Endocrinol. Metab. 295 2008 E678 E685
94. R. Boushel, E. Gnaiger, P. Schjerling, M. Skovbro, R. Kraunsoe, and F. Dela Patients with type 2 diabetes have normal mitochondrial function in skeletal muscle Diabetologia 50 2007 790 796
95. J.A. Hawley, and S.J. Lessard Mitochondrial function: use it or lose it Diabetologia 50 2007 699 702
96. P. Garcia-Roves, J.M. Huss, D.H. Han, C.R. Hancock, E. Iglesias-Gutierrez, M. Chen, and J.O. Holloszy Raising plasma fatty acid concentration induces increased biogenesis of mitochondria in skeletal muscle Proc. Natl. Acad. Sci. U. S. A. 104 2007 10709 10713
97. N. Turner, C.R. Bruce, S.M. Beale, K.L. Hoehn, T. So, M.S. Rolph, and G.J. Cooney Excess lipid availability increases mitochondrial fatty acid oxidative capacity in muscle: evidence against a role for reduced fatty acid oxidation in lipid-induced insulin resistance in rodents Diabetes 56 2007 2085 2092
98. J. de Wilde, R. Mohren, S. van den Berg, M. Boekschoten, K.W. Dijk, P. de Groot, M. Muller, E. Mariman, and E. Smit Short-term high fat-feeding results in morphological and metabolic adaptations in the skeletal muscle of C57BL/6J mice Physiol. Genomics 32 2008 360 369
99. C.R. Hancock, D.H. Han, M. Chen, S. Terada, T. Yasuda, D.C. Wright, and J.O. Holloszy High-fat diets cause insulin resistance despite an increase in muscle mitochondria Proc. Natl. Acad. Sci. U. S. A. 105 2008 7815 7820
100. C.R. Bruce, A.J. Hoy, N. Turner, M.J. Watt, T.L. Allen, K. Carpenter, G.J. Cooney, M.A. Febbraio, and E.W. Kraegen Overexpression of carnitine palmitoyltransferase-1 in skeletal muscle is sufficient to enhance fatty acid oxidation and improve high-fat diet-induced insulin resistance Diabetes 58 2009 550 558
101. N. Turner, K. Hariharan, J. TidAng, G. Frangioudakis, S.M. Beale, L.E. Wright, X.Y. Zeng, S.J. Leslie, J.Y. Li, E.W. Kraegen, G.J. Cooney, and J.M. Ye Enhancement of muscle mitochondrial oxidative capacity and alterations in insulin action are lipid species dependent: potent tissue-specific effects of medium-chain fatty acids Diabetes 58 2009 2547 2554
102. E.J. Stephenson, D.M. Camera, T.A. Jenkins, J.S. Lee, S. Kosari, J.A. Hawley, and N.K. Stepto Skeletal muscle respiratory capacity is enhanced in rats consuming an obesogenic Western diet Am. J. Physiol. Endocrinol. Metab. 302 2012 E1541-E1549
103. B.M. Forman, J. Chen, and R.M. Evans Hypolipidemic drugs, polyunsaturated fatty acids, and eicosanoids are ligands for peroxisome proliferator-activated receptors alpha and delta Proc. Natl. Acad. Sci. U. S. A. 94 1997 4312 4317
104. M. Schuler, F. Ali, C. Chambon, D. Duteil, J.M. Bornert, A. Tardivel, B. Desvergne, W. Wahli, P. Chambon, and D. Metzger PGC1alpha expression is controlled in skeletal muscles by PPARbeta, whose ablation results in fiber-type switching, obesity, and type 2 diabetes Cell Metab. 4 2006 407 414
105. E. Hondares, I. Pineda-Torra, R. Iglesias, B. Staels, F. Villarroya, and M. Giralt PPARdelta, but not PPARalpha, activates PGC-1alpha gene transcription in muscle Biochem. Biophys. Res. Commun. 354 2007 1021 1027
106. N.M. van den Broek, J. Ciapaite, H.M. De Feyter, S.M. Houten, R.J. Wanders, J.A. Jeneson, K. Nicolay, and J.J. Prompers Increased mitochondrial content rescues in vivo muscle oxidative capacity in long-term high-fat-diet-fed rats FASEB J. 24 2010 1354 1364
107. R. Sreekumar, J. Unnikrishnan, A. Fu, J. Nygren, K.R. Short, J. Schimke, R. Barazzoni, and K.S. Nair Impact of high-fat diet and antioxidant supplement on mitochondrial functions and gene transcripts in rat muscle Am. J. Physiol. Endocrinol. Metab. 282 2002 E1055 E1061
108. A. Masgrau, A. Mishellany-Dutour, H. Murakami, A.M. Beaufrere, S. Walrand, C. Giraudet, C. Migne, M. Gerbaix, L. Metz, D. Courteix, C. Guillet, and Y. Boirie Time-course changes of muscle protein synthesis associated with obesity-induced lipotoxicity J. Physiol. 590 2012 5199 5210
109. D. Samocha-Bonet, L.V. Campbell, T.A. Mori, K.D. Croft, J.R. Greenfield, N. Turner, and L.K. Heilbronn Overfeeding reduces insulin sensitivity and increases oxidative stress, without altering markers of mitochondrial content and function in humans PLoS One 7 2012 e36320
110. D.H. Han, L.A. Nolte, J.S. Ju, T. Coleman, J.O. Holloszy, and C.F. Semenkovich UCP-mediated energy depletion in skeletal muscle increases glucose transport despite lipid accumulation and mitochondrial dysfunction Am. J. Physiol. Endocrinol. Metab. 286 2004 E347 E353
111. A. Wredenberg, C. Freyer, M.E. Sandstrom, A. Katz, R. Wibom, H. Westerblad, and N.G. Larsson Respiratory chain dysfunction in skeletal muscle does not cause insulin resistance Biochem. Biophys. Res. Commun. 350 2006 202 207
112. J.A. Pospisilik, C. Knauf, N. Joza, P. Benit, M. Orthofer, P.D. Cani, I. Ebersberger, T. Nakashima, R. Sarao, G. Neely, H. Esterbauer, A. Kozlov, C.R. Kahn, G. Kroemer, P. Rustin, R. Burcelin, and J.M. Penninger Targeted deletion of AIF decreases mitochondrial oxidative phosphorylation and protects from obesity and diabetes Cell 131 2007 476 491
113. C. Zechner, L. Lai, J.F. Zechner, T. Geng, Z. Yan, J.W. Rumsey, D. Collia, Z. Chen, D.F. Wozniak, T.C. Leone, and D.P. Kelly Total skeletal muscle PGC-1 deficiency uncouples mitochondrial derangements from fiber type determination and insulin sensitivity Cell Metab. 12 2010 633 642
114. D.H. Han, C.R. Hancock, S.R. Jung, K. Higashida, S.H. Kim, and J.O. Holloszy Deficiency of the mitochondrial electron transport chain in muscle does not cause insulin resistance PLoS One 6 2011 e19739
115. S. Larsen, I. Ara, R. Rabol, J.L. Andersen, R. Boushel, F. Dela, and J.W. Helge Are substrate use during exercise and mitochondrial respiratory capacity decreased in arm and leg muscle in type 2 diabetes? Diabetologia 52 2009 1400 1408
116. R. Rabol, S. Larsen, P.M. Hojberg, T. Almdal, R. Boushel, S.B. Haugaard, J.L. Andersen, S. Madsbad, and F. Dela Regional anatomic differences in skeletal muscle mitochondrial respiration in type 2 diabetes and obesity J. Clin. Endocrinol. Metab. 95 2010 857 863
117. E.V. Menshikova, V.B. Ritov, F.G. Toledo, R.E. Ferrell, B.H. Goodpaster, and D.E. Kelley Effects of weight loss and physical activity on skeletal muscle mitochondrial function in obesity Am. J. Physiol. Endocrinol. Metab. 288 2005 E818 E825
118. F.G. Toledo, E.V. Menshikova, V.B. Ritov, K. Azuma, Z. Radikova, J. DeLany, and D.E. Kelley Effects of physical activity and weight loss on skeletal muscle mitochondria and relationship with glucose control in type 2 diabetes Diabetes 56 2007 2142 2147
119. J.R. Berggren, K.E. Boyle, W.H. Chapman, and J.A. Houmard Skeletal muscle lipid oxidation and obesity: influence of weight loss and exercise Am. J. Physiol. Endocrinol. Metab. 294 2008 E726 E732
120. M. Hey-Mogensen, K. Hojlund, B.F. Vind, L. Wang, F. Dela, H. Beck-Nielsen, M. Fernstrom, and K. Sahlin 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 2010 1976 1985
121. S. Bajpeyi, M. Pasarica, C. Moro, K. Conley, S. Jubrias, O. Sereda, D.H. Burk, Z. Zhang, A. Gupta, L. Kjems, and S.R. Smith Skeletal muscle mitochondrial capacity and insulin resistance in type 2 diabetes J. Clin. Endocrinol. Metab. 96 2011 1160 1168
122. C.R. Bruce, M.J. Anderson, A.L. Carey, D.G. Newman, A. Bonen, A.D. Kriketos, G.J. Cooney, and J.A. Hawley Muscle oxidative capacity is a better predictor of insulin sensitivity than lipid status J. Clin. Endocrinol. Metab. 88 2003 5444 5451
123. D.A. Hood, I. Irrcher, V. Ljubicic, and A.M. Joseph Coordination of metabolic plasticity in skeletal muscle J. Exp. Biol. 209 2006 2265 2275
124. C.R. Bruce, A.B. Thrush, V.A. Mertz, V. Bezaire, A. Chabowski, G.J. Heigenhauser, and D.J. Dyck Endurance training in obese humans improves glucose tolerance and mitochondrial fatty acid oxidation and alters muscle lipid content Am. J. Physiol. Endocrinol. Metab. 291 2006 E99 E107
125. R. Simonen, E. Levalahti, J. Kaprio, T. Videman, and M.C. Battie Multivariate genetic analysis of lifetime exercise and environmental factors Med. Sci. Sports Exerc. 36 2004 1559 1566
126. M. Gaster, and H. Beck-Nielsen The reduced insulin-mediated glucose oxidation in skeletal muscle from type 2 diabetic subjects may be of genetic origin - evidence from cultured myotubes Biochim. Biophys. Acta 1690 2004 85 91
127. M. Gaster, A.C. Rustan, V. Aas, and H. Beck-Nielsen Reduced lipid oxidation in skeletal muscle from type 2 diabetic subjects may be of genetic origin: evidence from cultured myotubes Diabetes 53 2004 542 548
128. B. Ukropcova, M. McNeil, O. Sereda, L. de Jonge, H. Xie, G.A. Bray, and S.R. Smith Dynamic changes in fat oxidation in human primary myocytes mirror metabolic characteristics of the donor J. Clin. Invest. 115 2005 1934 1941
129. R.R. Henry, L. Abrams, S. Nikoulina, and T.P. Ciaraldi Insulin action and glucose metabolism in nondiabetic control and NIDDM subjects. Comparison using human skeletal muscle cell cultures Diabetes 44 1995 936 946
130. R.R. Henry, T.P. Ciaraldi, S. Mudaliar, L. Abrams, and S.E. Nikoulina Acquired defects of glycogen synthase activity in cultured human skeletal muscle cells: influence of high glucose and insulin levels Diabetes 45 1996 400 407
131. D.M. Mott, C. Hoyt, R. Caspari, K. Stone, R. Pratley, and C. Bogardus Palmitate oxidation rate and action on glycogen synthase in myoblasts from insulin-resistant subjects Am. J. Physiol. Endocrinol. Metab. 279 2000 E561 E569
132. J.A. Houmard, W.J. Pories, and G.L. Dohm Is there a metabolic program in the skeletal muscle of obese individuals? J. Obes. 2011 2011 250496
133. C. Bouchard, P. An, T. Rice, J.S. Skinner, J.H. Wilmore, J. Gagnon, L. Perusse, A.S. Leon, and D.C. Rao Familial aggregation of VO(2max) response to exercise training: results from the HERITAGE Family Study J. Appl. Physiol. 87 1999 1003 1008
134. R.A. Howlett, N.C. Gonzalez, H.E. Wagner, Z. Fu, S.L. Britton, L.G. Koch, and P.D. Wagner Selected contribution: skeletal muscle capillarity and enzyme activity in rats selectively bred for running endurance J. Appl. Physiol. 94 2003 1682 1688
135. R.L. Simonen, L. Perusse, T. Rankinen, T. Rice, D.C. Rao, and C. Bouchard Familial aggregation of physical activity levels in the Quebec Family Study Med. Sci. Sports Exerc. 34 2002 1137 1142
136. J.H. Stubbe, D.I. Boomsma, J.M. Vink, B.K. Cornes, N.G. Martin, A. Skytthe, K.O. Kyvik, R.J. Rose, U.M. Kujala, J. Kaprio, J.R. Harris, N.L. Pedersen, J. Hunkin, T.D. Spector, and E.J. de Geus Genetic influences on exercise participation in 37,051 twin pairs from seven countries PLoS One 1 2006 e22
137. S.J. Elder, A.H. Lichtenstein, A.G. Pittas, S.B. Roberts, P.J. Fuss, A.S. Greenberg, M.A. McCrory, T.J. Bouchard Jr., E. Saltzman, and M.C. Neale Genetic and environmental influences on factors associated with cardiovascular disease and the metabolic syndrome J. Lipid Res. 50 2009 1917 1926
138. T. Leskinen, R. Rinnankoski-Tuikka, M. Rintala, T. Seppanen-Laakso, E. Pollanen, M. Alen, S. Sipila, J. Kaprio, V. Kovanen, P. Rahkila, M. Oresic, H. Kainulainen, and U.M. Kujala Differences in muscle and adipose tissue gene expression and cardio-metabolic risk factors in the members of physical activity discordant twin pairs PLoS One 5 2010
139. L. Mustelin, K.H. Pietilainen, A. Rissanen, A.R. Sovijarvi, P. Piirila, J. Naukkarinen, L. Peltonen, J. Kaprio, and H. Yki-Jarvinen Acquired obesity and poor physical fitness impair expression of genes of mitochondrial oxidative phosphorylation in monozygotic twins discordant for obesity Am. J. Physiol. Endocrinol. Metab. 295 2008 E148 E154
140. L. Mustelin, K. Silventoinen, K. Pietilainen, A. Rissanen, and J. Kaprio Physical activity reduces the influence of genetic effects on BMI and waist circumference: a study in young adult twins Int. J. Obes. 33 2009 29 36
141. M.S. Bray, J.M. Hagberg, L. Perusse, T. Rankinen, S.M. Roth, B. Wolfarth, and C. Bouchard The human gene map for performance and health-related fitness phenotypes: the 2006-2007 update Med. Sci. Sports Exerc. 41 2009 35 73
142. L.G. Koch, and S.L. Britton Artificial selection for intrinsic aerobic endurance running capacity in rats Physiol. Genomics 5 2001 45 52
143. U. Wisloff, S.M. Najjar, O. Ellingsen, P.M. Haram, S. Swoap, Q. Al-Share, M. Fernstrom, K. Rezaei, S.J. Lee, L.G. Koch, and S.L. Britton Cardiovascular
144. S.J. Lessard, D.A. Rivas, Z.P. Chen, B.J. van Denderen, M.J. Watt, L.G. Koch, S.L. Britton, B.E. Kemp, and J.A. Hawley Impaired skeletal muscle beta-adrenergic activation and lipolysis are associated with whole-body insulin resistance in rats bred for low intrinsic exercise capacity Endocrinology 150 2009 4883 4891
145. C.M. Novak, C. Escande, P.R. Burghardt, M. Zhang, M.T. Barbosa, E.N. Chini, S.L. Britton, L.G. Koch, H. Akil, and J.A. Levine Spontaneous activity, economy of activity, and resistance to diet-induced obesity in rats bred for high intrinsic aerobic capacity Horm. Behav. 58 2010 355 367
146. E.J. Stephenson, N.K. Stepto, L.G. Koch, S.L. Britton, and J.A. Hawley Divergent skeletal muscle respiratory capacities in rats artificially selected for high- and low-running ability: a role for Nor1? J. Appl. Physiol. 113 2012 1403 1412
147. E.J. Stephenson, S.J. Lessard, D.A. Rivas, M.J. Watt, B.B. Yaspelkis III, L.G. Koch, S.L. Britton, and J.A. Hawley Exercise training enhances white adipose tissue metabolism in rats selectively bred for low- or high-endurance running capacity Am. J. Physiol. Endocrinol. Metab. 2013 E429-E43
148. R.H. Ritchie, C.H. Leo, C. Qin, E.J. Stephenson, M.A. Bowden, K.D. Buxton, S.J. Lessard, D.A. Rivas, L.G. Koch, S.L. Britton, J.A. Hawley, and O.L. Woodman Low intrinsic exercise capacity in rats predisposes to age-dependent cardiac remodeling independent of macrovascular function Am. J. Physiol. Heart Circ. Physiol. 304 2013 H729 H739
149. D.A. Rivas, S.J. Lessard, M. Saito, A.M. Friedhuber, L.G. Koch, S.L. Britton, B.B. Yaspelkis III, and J.A. Hawley Low intrinsic running capacity is associated with reduced skeletal muscle substrate oxidation and lower mitochondrial content in white skeletal muscle Am. J. Physiol. Regul. Integr. Comp. Physiol. 300 2011 R835 R843
150. C.M. Novak, C. Escande, S.M. Gerber, E.N. Chini, M. Zhang, S.L. Britton, L.G. Koch, and J.A. Levine Endurance capacity, not body size, determines physical activity levels: role of skeletal muscle PEPCK PLoS One 4 2009 e5869
151. S.J. Lessard, D.A. Rivas, E.J. Stephenson, B.B. Yaspelkis III, L.G. Koch, S.L. Britton, and J.A. Hawley Exercise training reverses impaired skeletal muscle metabolism induced by artificial selection for low aerobic capacity Am. J. Physiol. Regul. Integr. Comp. Physiol. 300 2011 R175 R182