Implications of mitochondrial uncoupling in skeletal muscle in the development and treatment of obesity

FEBS Journal

Volumn 280, Issue 20, 2013, Pages 5015-5029

  Thrush, A Brianne ^a   Dent, Robert ^b   McPherson, Ruth ^a   Harper, Mary Ellen ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

Author keywords

diet resistance; mitochondria; obesity; oxidative phosphorylation; proton leak; uncoupling; weight loss

Indexed keywords

5,10 METHYLENETETRAHYDROFOLATE REDUCTASE (FADH2); ADENINE NUCLEOTIDE TRANSLOCASE; ADENOSINE TRIPHOSPHATE; BIOLOGICAL FACTOR; CATECHOLAMINE; CYTOSINE; FATTY ACID; LEPTIN; MITOCHONDRIAL PROTEIN; MITOFUSIN 1; NUCLEAR RESPIRATORY FACTOR 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; THYMINE; THYROID HORMONE; UNCOUPLING PROTEIN 1; UNCOUPLING PROTEIN 2; UNCOUPLING PROTEIN 3;

BASAL METABOLIC RATE; BODY WEIGHT; CONFERENCE PAPER; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENERGY BALANCE; ENERGY EXPENDITURE; ENERGY METABOLISM; EXERCISE; FATTY ACID OXIDATION; GENE; HETEROZYGOTE; HUMAN; MITOCHONDRIAL RESPIRATION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; OXIDATIVE PHOSPHORYLATION; OXIDATIVE PHOSPHORYLATION UNCOUPLING; PHYSICAL ACTIVITY; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RESTING METABOLIC RATE; SINGLE NUCLEOTIDE POLYMORPHISM; SKELETAL MUSCLE; UCP1 GENE; UCP2 GENE; UCP3 GENE; WEIGHT GAIN; WEIGHT REDUCTION;

DIET RESISTANCE; MITOCHONDRIA; OBESITY; OXIDATIVE PHOSPHORYLATION; PROTON LEAK; UNCOUPLING; WEIGHT LOSS;

ANIMALS; DIABETES MELLITUS, TYPE 2; ENERGY METABOLISM; EXERCISE; HUMANS; MITOCHONDRIA, MUSCLE; MUSCLE, SKELETAL; OBESITY; OXIDATIVE PHOSPHORYLATION; PROTONS; WEIGHT GAIN; WEIGHT LOSS;

EID: 84885293815     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12399     Document Type: Conference Paper

References (173)

1. Rossen L, &, Rossen EA, (2012) Obesity 101. Springer Publishing Co., LLC., New York.
2. Vucenik I, &, Stains JP, (2012) Obesity and cancer risk: evidence, mechanisms, and recommendations. Ann N Y Acad Sci 1271, 37-43.
3. World Health Organization (2012) World Health Statistics 2012.
4. Bouchard C, Tremblay A, Despres JP, Nadeau A, Lupien PJ, Theriault G, Dussault J, Moorjani S, Pinault S, &, Fournier G, (1990) The response to long-term overfeeding in identical twins. N Engl J Med 322, 1477-1482.
5. Bouchard C, Tremblay A, Despres JP, Theriault G, Nadeau A, Lupien PJ, Moorjani S, Prudhomme D, &, Fournier G, (1994) The response to exercise with constant energy intake in identical twins. Obes Res 2, 400-410.
6. Harper ME, Dent R, Monemdjou S, Bezaire V, Van Wyck L, Wells G, Kavaslar GN, Gauthier A, Tesson F, &, McPherson R, (2002) Decreased mitochondrial proton leak and reduced expression of uncoupling protein 3 in skeletal muscle of obese diet-resistant women. Diabetes 51, 2459-2466.
7. Burcelin R, (2012) Regulation of metabolism: a cross talk between gut microbiota and its human host. Physiology 27, 300-307.
8. Ravussin E, Lillioja S, Anderson TE, Christin L, &, Bogardus C, (1986) Determinants of 24-hour energy expenditure in man. Methods and results using a respiratory chamber. J Clin Invest 78, 1568-1578.
9. Dubois EF, Ebaugh FG Jr, &, Hardy JD, (1952) Basal heat production and elimination of thirteen normal women at temperatures from 22 degrees C. to 35 degrees C. J Nutr 48, 257-293.
10. Wilkerson JE, Raven PB, &, Horvath SM, (1972) Critical temperature of unacclimatized male Caucasians. J Appl Physiol 33, 451-455.
11. Henry CJ, (2005) Basal metabolic rate studies in humans: measurement and development of new equations. Public Health Nutr 8, 1133-1152.
12. Levine JA, (2004) Nonexercise activity thermogenesis (NEAT): environment and biology. Am J Physiol Endocrinol Metab 286, E675-E685.
13. Johnstone AM, Murison SD, Duncan JS, Rance KA, &, Speakman JR, (2005) Factors influencing variation in basal metabolic rate include fat-free mass, fat mass, age, and circulating thyroxine but not sex, circulating leptin, or triiodothyronine. Am J Clin Nutr 82, 941-948.
14. Harper ME, &, Seifert EL, (2008) Thyroid hormone effects on mitochondrial energetics. Thyroid 18, 145-156.
15. Butte NF, Hopkinson JM, Mehta N, Moon JK, &, Smith EO, (1999) Adjustments in energy expenditure and substrate utilization during late pregnancy and lactation. Am J Clin Nutr 69, 299-307.
16. Grande F, Anderson JT, &, Keys A, (1958) Changes of basal metabolic rate in man in semistarvation and refeeding. J Appl Physiol 12, 230-238.
17. Fukagawa NK, Bandini LG, &, Young JB, (1990) Effect of age on body composition and resting metabolic rate. Am J Physiol 259, E233-E238.
18. Leibel RL, Rosenbaum M, &, Hirsch J, (1995) Changes in energy expenditure resulting from altered body weight. N Engl J Med 332, 621-628.
19. Rosenbaum M, Hirsch J, Gallagher DA, &, Leibel RL, (2008) Long-term persistence of adaptive thermogenesis in subjects who have maintained a reduced body weight. Am J Clin Nutr 88, 906-912.
20. Martin CK, Heilbronn LK, de Jonge L, DeLany JP, Volaufova J, Anton SD, Redman LM, Smith SR, &, Ravussin E, (2007) Effect of calorie restriction on resting metabolic rate and spontaneous physical activity. Obesity (Silver Spring) 15, 2964-2973.
21. Ravussin E, &, Bogardus C, (1992) A brief overview of human energy metabolism and its relationship to essential obesity. Am J Clin Nutr 55, 242S-245S.
22. Rolfe DF, &, Brown GC, (1997) Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev 77, 731-758.
23. Harper ME, Green K, &, Brand MD, (2008) The efficiency of cellular energy transduction and its implications for obesity. Annu Rev Nutr 28, 13-33.
24. Muller AF, Fullwood L, Hawkins M, &, Cowley AJ, (1992) The integrated response of the cardiovascular system to food. Digestion 52, 184-193.
25. Sidery MB, &, Macdonald IA, (1994) The effect of meal size on the cardiovascular responses to food ingestion. Br J Nutr 71, 835-848.
26. van Baak MA, (2008) Meal-induced activation of the sympathetic nervous system and its cardiovascular and thermogenic effects in man. Physiol Behav 94, 178-186.
27. Tappy L, (1996) Thermic effect of food and sympathetic nervous system activity in humans. Reprod Nutr Dev 36, 391-397.
28. Astrup A, Andersen T, Christensen NJ, Bulow J, Madsen J, Breum L, &, Quaade F, (1990) Impaired glucose-induced thermogenesis and arterial norepinephrine response persist after weight reduction in obese humans. Am J Clin Nutr 51, 331-337.
29. Jung RT, Shetty PS, James WP, Barrand MA, &, Callingham BA, (1979) Reduced thermogenesis in obesity. Nature 279, 322-323.
30. Garland T Jr, Schutz H, Chappell MA, Keeney BK, Meek TH, Copes LE, Acosta W, Drenowatz C, Maciel RC, van Dijk G, et al,. (2011) The biological control of voluntary exercise, spontaneous physical activity and daily energy expenditure in relation to obesity: human and rodent perspectives. J Exp Biol 214, 206-229.
31. Levine JA, Eberhardt NL, &, Jensen MD, (1999) Role of nonexercise activity thermogenesis in resistance to fat gain in humans. Science 283, 212-214.
32. Field J, Belding HS, &, Martin A, (1939) An analysis of the relation between basal metabolism and summated tissue respiraton in the rat. J Cell Comp Physiol 14, 143-155.
33. Rolfe DF, &, Brand MD, (1996) Contribution of mitochondrial proton leak to skeletal muscle respiration and to standard metabolic rate. Am J Physiol 271, C1380-C1389.
34. Rich P, (2003) Chemiosmotic coupling: the cost of living. Nature 421, 583.
35. Brand MD, Harper ME, &, Taylor HC, (1993) Control of the effective P/O ratio of oxidative phosphorylation in liver mitochondria and hepatocytes. Biochem J 291, 739-748.
36. Divakaruni AS, &, Brand MD, (2011) The regulation and physiology of mitochondrial proton leak. Physiology 26, 192-205.
37. Rolfe DF, Newman JM, Buckingham JA, Clark MG, &, Brand MD, (1999) Contribution of mitochondrial proton leak to respiration rate in working skeletal muscle and liver and to SMR. Am J Physiol 276, C692-C699.
38. Zurlo F, Larson K, Bogardus C, &, Ravussin E, (1990) Skeletal muscle metabolism is a major determinant of resting energy expenditure. J Clin Invest 86, 1423-1427.
39. Brand MD, Pakay JL, Ocloo A, Kokoszka J, Wallace DC, Brookes PS, &, Cornwall EJ, (2005) The basal proton conductance of mitochondria depends on adenine nucleotide translocase content. Biochem J 392, 353-362.
40. Echtay KS, Esteves TC, Pakay JL, Jekabsons MB, Lambert AJ, Portero-Otin M, Pamplona R, Vidal-Puig AJ, Wang S, Roebuck SJ, et al,. (2003) A signalling role for 4-hydroxy-2-nonenal in regulation of mitochondrial uncoupling. EMBO J 22, 4103-4110.
41. Andreyev A, Bondareva TO, Dedukhova VI, Mokhova EN, Skulachev VP, &, Volkov NI, (1988) Carboxyatractylate inhibits the uncoupling effect of free fatty acids. FEBS Lett 226, 265-269.
42. Nicholls DG, &, Rial E, (1999) A history of the first uncoupling protein, UCP1. J Bioenerg Biomembr 31, 399-406.
43. Himms-Hagen J, (1970) Regulation of metabolic processes in brown adipose tissue in relation to nonshivering thermogenesis. Adv Enzyme Regul 8, 131-151.
44. Li B, Nolte LA, Ju JS, Han DH, Coleman T, Holloszy JO, &, Semenkovich CF, (2000) Skeletal muscle respiratory uncoupling prevents diet-induced obesity and insulin resistance in mice. Nat Med 6, 1115-1120.
45. Heaton JM, (1972) The distribution of brown adipose tissue in the human. J Anat 112, 35-39.
46. Cannon B, &, Nedergaard J, (2004) Brown adipose tissue: function and physiological significance. Physiol Rev 84, 277-359.
47. Virtanen KA, Lidell ME, Orava J, Heglind M, Westergren R, Niemi T, Taittonen M, Laine J, Savisto NJ, Enerback S, et al,. (2009) Functional brown adipose tissue in healthy adults. N Engl J Med 360, 1518-1525.
48. Huttunen P, Hirvonen J, &, Kinnula V, (1981) The occurrence of brown adipose tissue in outdoor workers. Eur J Appl Physiol Occup Physiol 46, 339-345.
49. Azzu V, &, Brand MD, (2010) The on-off switches of the mitochondrial uncoupling proteins. Trends Biochem Sci 35, 298-307.
50. Brand MD, (2000) Uncoupling to survive? The role of mitochondrial inefficiency in ageing Exp Gerontol 35, 811-820.
51. Arsenijevic D, Onuma H, Pecqueur C, Raimbault S, Manning BS, Miroux B, Couplan E, Alves-Guerra MC, Goubern M, Surwit R, et al,. (2000) Disruption of the uncoupling protein-2 gene in mice reveals a role in immunity and reactive oxygen species production. Nat Genet 26, 435-439.
52. Vidal-Puig AJ, Grujic D, Zhang CY, Hagen T, Boss O, Ido Y, Szczepanik A, Wade J, Mootha V, Cortright R, et al,. (2000) Energy metabolism in uncoupling protein 3 gene knockout mice. J Biol Chem 275, 16258-16266.
53. Seifert EL, Bezaire V, Estey C, &, Harper ME, (2008) Essential role for uncoupling protein-3 in mitochondrial adaptation to fasting but not in fatty acid oxidation or fatty acid anion export. J Biol Chem 283, 25124-25131.
54. Nabben M, Hoeks J, Briede JJ, Glatz JF, Moonen-Kornips E, Hesselink MK, &, Schrauwen P, (2008) The effect of UCP3 overexpression on mitochondrial ROS production in skeletal muscle of young versus aged mice. FEBS Lett 582, 4147-4152.
55. Costford SR, Chaudhry SN, Salkhordeh M, &, Harper ME, (2006) Effects of the presence, absence, and overexpression of uncoupling protein-3 on adiposity and fuel metabolism in congenic mice. Am J Physiol Endocrinol Metab 290, E1304-E1312.
56. Costford SR, Seifert EL, Bezaire V, &, Gerrits MF, Bevilacqua L, Gowing A, &, Harper ME, (2007) The energetic implications of uncoupling protein-3 in skeletal muscle. Appl Physiol Nutr Metab 32, 884-894.
57. Son C, Hosoda K, Ishihara K, Bevilacqua L, Masuzaki H, Fushiki T, Harper ME, &, Nakao K, (2004) Reduction of diet-induced obesity in transgenic mice overexpressing uncoupling protein 3 in skeletal muscle. Diabetologia 47, 47-54.
58. Costford SR, Chaudhry SN, Crawford SA, Salkhordeh M, &, Harper ME, (2008) Long-term high-fat feeding induces greater fat storage in mice lacking UCP3. Am J Physiol Endocrinol Metab 295, E1018-E1024.
59. Fink BD, Herlein JA, Almind K, Cinti S, Kahn CR, &, Sivitz WI, (2007) Mitochondrial proton leak in obesity-resistant and obesity-prone mice. Am J Physiol Regul Integr Comp Physiol 293, R1773-R1780.
60. Nabben M, Hoeks J, Moonen-Kornips E, van Beurden D, Briede JJ, Hesselink MK, Glatz JF, &, Schrauwen P, (2011) Significance of uncoupling protein 3 in mitochondrial function upon mid- and long-term dietary high-fat exposure. FEBS Lett 585, 4010-4017.
61. Ukkola O, Tremblay A, Sun G, Chagnon YC, &, Bouchard C, (2001) Genetic variation at the uncoupling protein 1, 2 and 3 loci and the response to long-term overfeeding. Eur J Clin Nutr 55, 1008-1015.
62. Fumeron F, Durack-Bown I, Betoulle D, Cassard-Doulcier AM, Tuzet S, Bouillaud F, Melchior JC, Ricquier D, &, Apfelbaum M, (1996) Polymorphisms of uncoupling protein (UCP) and beta 3 adrenoreceptor genes in obese people submitted to a low calorie diet. Int J Obes Relat Metab Disord 20, 1051-1054.
63. Kogure A, Yoshida T, Sakane N, Umekawa T, Takakura Y, &, Kondo M, (1998) Synergic effect of polymorphisms in uncoupling protein 1 and beta3-adrenergic receptor genes on weight loss in obese Japanese. Diabetologia 41, 1399.
64. Oppert JM, Vohl MC, Chagnon M, Dionne FT, Cassard-Doulcier AM, Ricquier D, Perusse L, &, Bouchard C, (1994) DNA polymorphism in the uncoupling protein (UCP) gene and human body fat. Int J Obes Relat Metab Disord 18, 526-531.
65. Jia JJ, Tian YB, Cao ZH, Tao LL, Zhang X, Gao SZ, Ge CR, Lin QY, &, Jois M, (2010) The polymorphisms of UCP1 genes associated with fat metabolism, obesity and diabetes. Mol Biol Rep 37, 1513-1522.
66. Jia JJ, Zhang X, Ge CR, &, Jois M, (2009) The polymorphisms of UCP2 and UCP3 genes associated with fat metabolism, obesity and diabetes. Obes Rev 10, 519-526.
67. Esterbauer H, Schneitler C, Oberkofler H, Ebenbichler C, Paulweber B, Sandhofer F, Ladurner G, Hell E, Strosberg AD, Patsch JR, et al,. (2001) A common polymorphism in the promoter of UCP2 is associated with decreased risk of obesity in middle-aged humans. Nat Genet 28, 178-183.
68. Krempler F, Esterbauer H, Weitgasser R, Ebenbichler C, Patsch JR, Miller K, Xie M, Linnemayr V, Oberkofler H, &, Patsch W, (2002) A functional polymorphism in the promoter of UCP2 enhances obesity risk but reduces type 2 diabetes risk in obese middle-aged humans. Diabetes 51, 3331-3335.
69. Gable DR, Stephens JW, Cooper JA, Miller GJ, &, Humphries SE, (2006) Variation in the UCP2-UCP3 gene cluster predicts the development of type 2 diabetes in healthy middle-aged men. Diabetes 55, 1504-1511.
70. Schrauwen P, Xia J, Walder K, Snitker S, &, Ravussin E, (1999) A novel polymorphism in the proximal UCP3 promoter region: effect on skeletal muscle UCP3 mRNA expression and obesity in male non-diabetic Pima Indians. Int J Obes Relat Metab Disord 23, 1242-1245.
71. Kimm SY, Glynn NW, Aston CE, Damcott CM, Poehlman ET, Daniels SR, &, Ferrell RE, (2002) Racial differences in the relation between uncoupling protein genes and resting energy expenditure. Am J Clin Nutr 75, 714-719.
72. Lindholm E, Klannemark M, Agardh E, Groop L, &, Agardh CD, (2004) Putative role of polymorphisms in UCP1-3 genes for diabetic nephropathy. J Diabetes Complications 18, 103-107.
73. Bulotta A, Ludovico O, Coco A, Di Paola R, Quattrone A, Carella M, Pellegrini F, Prudente S, &, Trischitta V, (2005) The common -866G/A polymorphism in the promoter region of the UCP-2 gene is associated with reduced risk of type 2 diabetes in Caucasians from Italy. J Clin Endocrinol Metab 90, 1176-1180.
74. DuBois E, (1936) Basal Metabolism in Health and Disease. Lea and Febiger, Philadelphia.
75. Tomasi TE, (1991) Utilization rates of thyroid hormones in mammals. Comp Biochem Physiol A Comp Physiol 100, 503-516.
76. Ardail D, Lerme F, Puymirat J, &, Morel G, (1993) Evidence for the presence of alpha and beta-related T3 receptors in rat liver mitochondria. Eur J Cell Biol 62, 105-113.
77. Wrutniak C, Cassar-Malek I, Marchal S, Rascle A, Heusser S, Keller JM, Flechon J, Dauca M, Samarut J, Ghysdael J, et al,. (1995) A 43-kDa protein related to c-Erb A alpha 1 is located in the mitochondrial matrix of rat liver. J Biol Chem 270, 16347-16354.
78. Morrish F, Buroker NE, Ge M, Ning XH, Lopez-Guisa J, Hockenbery D, &, Portman MA, (2006) Thyroid hormone receptor isoforms localize to cardiac mitochondrial matrix with potential for binding to receptor elements on mtDNA. Mitochondrion 6, 143-148.
79. Weitzel JM, Iwen KA, &, Seitz HJ, (2003) Regulation of mitochondrial biogenesis by thyroid hormone. Exp Physiol 88, 121-128.
80. Irrcher I, Adhihetty PJ, Sheehan T, Joseph AM, &, Hood DA, (2003) PPARgamma coactivator-1alpha expression during thyroid hormone- and contractile activity-induced mitochondrial adaptations. Am J Physiol Cell Physiol 284, C1669-C1677.
81. Scheller K, &, Sekeris CE, (2003) The effects of steroid hormones on the transcription of genes encoding enzymes of oxidative phosphorylation. Exp Physiol 88, 129-140.
82. Seitz HJ, Muller MJ, &, Soboll S, (1985) Rapid thyroid-hormone effect on mitochondrial and cytosolic ATP/ADP ratios in the intact liver cell. Biochem J 227, 149-153.
83. Rebuffe-Scrive M, Anderson B, Olbe L, &, Bjorntorp P, (1990) Metabolism of adipose tissue in intraabdominal depots in severely obese men and women. Metabolism 39, 1021-1025.
84. Hafner RP, &, Brand MD, (1988) Hypothyroidism in rats does not lower mitochondrial ADP/O and H+/O ratios. Biochem J 250, 477-484.
85. Harper ME, &, Brand MD, (1994) Hyperthyroidism stimulates mitochondrial proton leak and ATP turnover in rat hepatocytes but does not change the overall kinetics of substrate oxidation reactions. Can J Physiol Pharmacol 72, 899-908.
86. Harper ME, &, Brand MD, (1993) The quantitative contributions of mitochondrial proton leak and ATP turnover reactions to the changed respiration rates of hepatocytes from rats of different thyroid status. J Biol Chem 268, 14850-14860.
87. Nobes CD, Brown GC, Olive PN, &, Brand MD, (1990) Non-ohmic proton conductance of the mitochondrial inner membrane in hepatocytes. J Biol Chem 265, 12903-12909.
88. Mitchell CS, Savage DB, Dufour S, Schoenmakers N, Murgatroyd P, Befroy D, Halsall D, Northcott S, Raymond-Barker P, Curran S, et al,. (2010) Resistance to thyroid hormone is associated with raised energy expenditure, muscle mitochondrial uncoupling, and hyperphagia. J Clin Invest 120, 1345-1354.
89. Hagopian K, Harper ME, Ram JJ, Humble SJ, Weindruch R, &, Ramsey JJ, (2005) Long-term calorie restriction reduces proton leak and hydrogen peroxide production in liver mitochondria. Am J Physiol Endocrinol Metab 288, E674-E684.
90. Bevilacqua L, Ramsey JJ, Hagopian K, Weindruch R, &, Harper ME, (2005) Long-term caloric restriction increases UCP3 content but decreases proton leak and reactive oxygen species production in rat skeletal muscle mitochondria. Am J Physiol Endocrinol Metab 289, E429-E438.
91. Bevilacqua L, Ramsey JJ, Hagopian K, Weindruch R, &, Harper ME, (2004) Effects of short- and medium-term calorie restriction on muscle mitochondrial proton leak and reactive oxygen species production. Am J Physiol Endocrinol Metab 286, E852-E861.
92. Asami DK, McDonald RB, Hagopian K, Horwitz BA, Warman D, Hsiao A, Warden C, &, Ramsey JJ, (2008) Effect of aging, caloric restriction, and uncoupling protein 3 (UCP3) on mitochondrial proton leak in mice. Exp Gerontol 43, 1069-1076.
93. Raffaella C, Francesca B, Italia F, Marina P, Giovanna L, &, Susanna I, (2008) Alterations in hepatic mitochondrial compartment in a model of obesity and insulin resistance. Obesity (Silver Spring) 16, 958-964.
94. Ciapaite J, Bakker SJ, Van Eikenhorst G, Wagner MJ, Teerlink T, Schalkwijk CG, Fodor M, Ouwens DM, Diamant M, Heine RJ, et al,. (2007) Functioning of oxidative phosphorylation in liver mitochondria of high-fat diet fed rats. Biochim Biophys Acta 1772, 307-316.
95. Almind K, Manieri M, Sivitz WI, Cinti S, &, Kahn CR, (2007) Ectopic brown adipose tissue in muscle provides a mechanism for differences in risk of metabolic syndrome in mice. Proc Natl Acad Sci USA 104, 2366-2371.
96. Rabol R, Hojberg PM, Almdal T, Boushel R, Haugaard SB, Madsbad S, &, Dela F, (2009) Improved glycaemic control decreases inner mitochondrial membrane leak in type 2 diabetes. Diabetes Obes Metab 11, 355-360.
97. Boudina S, Sena S, Theobald H, Sheng X, Wright JJ, Hu XX, Aziz S, Johnson JI, Bugger H, Zaha VG, et al,. (2007) Mitochondrial energetics in the heart in obesity-related diabetes: direct evidence for increased uncoupled respiration and activation of uncoupling proteins. Diabetes 56, 2457-2466.
98. Zoll J, Sanchez H, N'Guessan B, Ribera F, Lampert E, Bigard X, Serrurier B, Fortin D, Geny B, Veksler V, et al,. (2002) Physical activity changes the regulation of mitochondrial respiration in human skeletal muscle. J Physiol 543, 191-200.
99. Conley KE, Amara CE, Bajpeyi S, Costford SR, Murray K, Jubrias SA, Arakaki L, Marcinek DJ, &, Smith SR, (2013) Higher mitochondrial respiration and uncoupling with reduced electron transport chain content in vivo in muscle of sedentary versus active subjects. J Clin Endocrinol Metab 98, 129-136.
100. Befroy DE, Petersen KF, Dufour S, Mason GF, Rothman DL, &, Shulman GI, (2008) Increased substrate oxidation and mitochondrial uncoupling in skeletal muscle of endurance-trained individuals. Proc Natl Acad Sci USA 105, 16701-16706.
101. Das SK, Gilhooly CH, Golden JK, Pittas AG, Fuss PJ, Dallal GE, McCrory MA, Saltzman E, &, Roberts SB, (2007) Long term effects of energy-restricted diets differing in glycemic load on metabolic adaptation and body composition. Open Nutr J 85, 1023-1030.
102. Doucet E, St-Pierre S, Almeras N, Despres JP, Bouchard C, &, Tremblay A, (2001) Evidence for the existence of adaptive thermogenesis during weight loss. Br J Nutr 85, 715-723.
103. Johannsen DL, Knuth ND, Huizenga R, Rood JC, Ravussin E, &, Hall KD, (2012) Metabolic slowing with massive weight loss despite preservation of fat-free mass. J Clin Endocrinol Metab 97, 2489-2496.
104. Doucet E, Imbeault P, St-Pierre S, Almeras N, Mauriege P, Despres JP, Bouchard C, &, Tremblay A, (2003) Greater than predicted decrease in energy expenditure during exercise after body weight loss in obese men. Clin Sci (Lond) 105, 89-95.
105. Harris JA, &, Benedict FG, (1918) A biometric study of human basal metabolism. Proc Natl Acad Sci USA 4, 370-373.
106. Frankenfield DC, (2013) Bias and accuracy of resting metabolic rate equations in non-obese and obese adults. Clin Nutr doi: 10.1016/j.clnu.2013.03. 022.
107. Westerterp KR, Meijer GA, Schoffelen P, &, Janssen EM, (1994) Body mass, body composition and sleeping metabolic rate before, during and after endurance training. Eur J Appl Physiol Occup Physiol 69, 203-208.
108. Schwartz A, Kuk JL, Lamothe G, &, Doucet E, (2012) Greater than predicted decrease in resting energy expenditure and weight loss: results from a systematic review. Obesity (Silver Spring) 20, 2307-2310.
109. Rosenbaum M, &, Leibel RL, (2010) Adaptive thermogenesis in humans. Int J Obes (Lond) 34 (Suppl 1), S47-S55.
110. Thomas DM, Bouchard C, Church T, Slentz C, Kraus WE, Redman LM, Martin CK, Silva AM, Vossen M, Westerterp K, et al,. (2012) Why do individuals not lose more weight from an exercise intervention at a defined dose? An energy balance analysis Obes Rev 13, 835-847.
111. Chaput JP, Drapeau V, Hetherington M, Lemieux S, Provencher V, &, Tremblay A, (2007) Psychobiological effects observed in obese men experiencing body weight loss plateau. Depress Anxiety 24, 518-521.
112. Kissileff HR, Thornton JC, Torres MI, Pavlovich K, Mayer LS, Kalari V, Leibel RL, &, Rosenbaum M, (2012) Leptin reverses declines in satiation in weight-reduced obese humans. Am J Clin Nutr 95, 309-317.
113. Rosenbaum M, Kissileff HR, Mayer LE, Hirsch J, &, Leibel RL, (2010) Energy intake in weight-reduced humans. Brain Res 1350, 95-102.
114. Rosenbaum M, Sy M, Pavlovich K, Leibel RL, &, Hirsch J, (2008) Leptin reverses weight loss-induced changes in regional neural activity responses to visual food stimuli. J Clin Invest 118, 2583-2591.
115. Hinkle W, Cordell M, Leibel R, Rosenbaum M, &, Hirsch J, (2013) Effects of reduced weight maintenance and leptin repletion on functional connectivity of the hypothalamus in obese humans. PLoS One 8, e59114.
116. Rosenbaum M, Hirsch J, Murphy E, &, Leibel RL, (2000) Effects of changes in body weight on carbohydrate metabolism, catecholamine excretion, and thyroid function. Am J Clin Nutr 71, 1421-1432.
117. Doucet E, St Pierre S, Almeras N, Mauriege P, Richard D, &, Tremblay A, (2000) Changes in energy expenditure and substrate oxidation resulting from weight loss in obese men and women: is there an important contribution of leptin? J Clin Endocrinol Metab 85, 1550-1556.
118. Rosenbaum M, Goldsmith R, Bloomfield D, Magnano A, Weimer L, Heymsfield S, Gallagher D, Mayer L, Murphy E, &, Leibel RL, (2005) Low-dose leptin reverses skeletal muscle, autonomic, and neuroendocrine adaptations to maintenance of reduced weight. J Clin Invest 115, 3579-3586.
119. Rabol R, Svendsen PF, Skovbro M, Boushel R, Haugaard SB, Schjerling P, Schrauwen P, Hesselink MK, Nilas L, Madsbad S, et al,. (2009) Reduced skeletal muscle mitochondrial respiration and improved glucose metabolism in nondiabetic obese women during a very low calorie dietary intervention leading to rapid weight loss. Metabolism 58, 1145-1152.
120. Dent R, Mcpherson R, &, Harper ME, (1999) Variability in weight loss in highly compliant women on a controlled dietary regimen. Obes Res 7 (Suppl), 1.
121. Gerrits MF, Ghosh S, Kavaslar N, Hill B, Tour A, Seifert EL, Beauchamp B, Gorman S, Stuart J, Dent R, et al,. (2010) Distinct skeletal muscle fiber characteristics and gene expression in diet-sensitive versus diet-resistant obesity. J Lipid Res 51, 2394-2404.
122. Mogensen M, Sahlin K, Fernstrom M, Glintborg D, Vind BF, Beck-Nielsen H, &, Hojlund K, (2007) Mitochondrial respiration is decreased in skeletal muscle of patients with type 2 diabetes. Diabetes 56, 1592-1599.
123. Sun G, Ukkola O, Rankinen T, Joanisse DR, &, Bouchard C, (2002) Skeletal muscle characteristics predict body fat gain in response to overfeeding in never-obese young men. Metabolism 51, 451-456.
124. Ghosh S, Dent R, Harper ME, Stuart J, &, McPherson R, (2011) Blood gene expression reveal pathway differences between diet-sensitive and resistant obese subjects prior to caloric restriction. Obesity (Silver Spring) 19, 457-463.
125. Bonen A, Parolin ML, Steinberg GR, Calles-Escandon J, Tandon NN, Glatz JF, Luiken JJ, Heigenhauser GJ, &, Dyck DJ, (2004) Triacylglycerol accumulation in human obesity and type 2 diabetes is associated with increased rates of skeletal muscle fatty acid transport and increased sarcolemmal FAT/CD36. FASEB J 18, 1144-1146.
126. Goodpaster BH, He J, Watkins S, &, Kelley DE, (2001) Skeletal muscle lipid content and insulin resistance: evidence for a paradox in endurance-trained athletes. J Clin Endocrinol Metab 86, 5755-5761.
127. Furukawa S, Fujita T, Shimabukuro M, Iwaki M, Yamada Y, Nakajima Y, Nakayama O, Makishima M, Matsuda M, &, Shimomura I, (2004) Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest 114, 1752-1761.
128. Keaney JF Jr, Larson MG, Vasan RS, Wilson PW, Lipinska I, Corey D, Massaro JM, Sutherland P, Vita JA, Benjamin EJ, et al,. (2003) Obesity and systemic oxidative stress: clinical correlates of oxidative stress in the Framingham Study. Arterioscler Thromb Vasc Biol 23, 434-439.
129. Chavez JA, Knotts TA, Wang LP, Li G, Dobrowsky RT, Florant GL, &, Summers SA, (2003) A role for ceramide, but not diacylglycerol, in the antagonism of insulin signal transduction by saturated fatty acids. J Biol Chem 278, 10297-10303.
130. Itani SI, Ruderman NB, Schmieder F, &, Boden G, (2002) Lipid-induced insulin resistance in human muscle is associated with changes in diacylglycerol, protein kinase C, and IkappaB-alpha. Diabetes 51, 2005-2011.
131. Dresner A, Laurent D, Marcucci M, Griffin ME, Dufour S, Cline GW, Slezak LA, Andersen DK, Hundal RS, Rothman DL, et al,. (1999) Effects of free fatty acids on glucose transport and IRS-1-associated phosphatidylinositol 3-kinase activity. J Clin Invest 103, 253-259.
132. Schmitz-Peiffer C, Craig DL, &, Biden TJ, (1999) Ceramide generation is sufficient to account for the inhibition of the insulin-stimulated PKB pathway in C2C12 skeletal muscle cells pretreated with palmitate. J Biol Chem 274, 24202-24210.
133. Kelley DE, He J, Menshikova EV, &, Ritov VB, (2002) Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 51, 2944-2950.
134. Kim JY, Hickner RC, Cortright RL, Dohm GL, &, Houmard JA, (2000) Lipid oxidation is reduced in obese human skeletal muscle. Am J Physiol Endocrinol Metab 279, E1039-E1044.
135. Simoneau JA, Veerkamp JH, Turcotte LP, &, Kelley DE, (1999) 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, 2051-2060.
136. Steinberg GR, Parolin ML, Heigenhauser GJ, &, Dyck DJ, (2002) Leptin increases FA oxidation in lean but not obese human skeletal muscle: evidence of peripheral leptin resistance. Am J Physiol Endocrinol Metab 283, E187-E192.
137. Holloway GP, Thrush AB, Heigenhauser GJ, Tandon NN, Dyck DJ, Bonen A, &, Spriet LL, (2007) Skeletal muscle mitochondrial FAT/CD36 content and palmitate oxidation are not decreased in obese women. Am J Physiol Endocrinol Metab 292, E1782-E1789.
138. Holloway GP, Benton CR, Mullen KL, Yoshida Y, Snook LA, Han XX, Glatz JF, Luiken JJ, Lally J, Dyck DJ, et al,. (2009) In obese rat muscle transport of palmitate is increased and is channeled to triacylglycerol storage despite an increase in mitochondrial palmitate oxidation. Am J Physiol Endocrinol Metab 296, E738-E747.
139. Hulver MW, Berggren JR, Cortright RN, Dudek RW, Thompson RP, Pories WJ, MacDonald KG, Cline GW, Shulman GI, Dohm GL, et al,. (2003) Skeletal muscle lipid metabolism with obesity. Am J Physiol Endocrinol Metab 284, E741-E747.
140. Boushel R, Gnaiger E, Schjerling P, Skovbro M, Kraunsoe R, &, Dela F, (2007) Patients with type 2 diabetes have normal mitochondrial function in skeletal muscle. Diabetologia 50, 790-796.
141. Ritov VB, Menshikova EV, He J, Ferrell RE, Goodpaster BH, &, Kelley DE, (2005) Deficiency of subsarcolemmal mitochondria in obesity and type 2 diabetes. Diabetes 54, 8-14.
142. Patti ME, Butte AJ, Crunkhorn S, Cusi K, Berria R, Kashyap S, Miyazaki Y, Kohane I, Costello M, Saccone R, 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, 8466-8471.
143. Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, Lehar J, Puigserver P, Carlsson E, Ridderstrale M, Laurila E, et al,. (2003) PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 34, 267-273.
144. Bell JA, Reed MA, Consitt LA, Martin OJ, Haynie KR, Hulver MW, Muoio DM, &, Dohm GL, (2010) Lipid partitioning, incomplete fatty acid oxidation, and insulin signal transduction in primary human muscle cells: effects of severe obesity, fatty acid incubation, and fatty acid translocase/CD36 overexpression. J Clin Endocrinol Metab 95, 3400-3410.
145. Thyfault JP, Cree MG, Zheng D, Zwetsloot JJ, Tapscott EB, Koves TR, Ilkayeva O, Wolfe RR, Muoio DM, &, Dohm GL, (2007) Contraction of insulin-resistant muscle normalizes insulin action in association with increased mitochondrial activity and fatty acid catabolism. Am J Physiol Cell Physiol 292, C729-C739.
146. Koves TR, Ussher JR, Noland RC, Slentz D, Mosedale M, Ilkayeva O, Bain J, Stevens R, Dyck JR, Newgard CB, et al,. (2008) Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance. Cell Metab 7, 45-56.
147. Cogswell AM, Stevens RJ, &, Hood DA, (1993) Properties of skeletal muscle mitochondria isolated from subsarcolemmal and intermyofibrillar regions. Am J Physiol 264, C383-C389.
148. Hood DA, (2001) Invited Review: contractile activity-induced mitochondrial biogenesis in skeletal muscle. J Appl Physiol 90, 1137-1157.
149. Benton CR, Nickerson JG, Lally J, Han XX, Holloway GP, Glatz JF, Luiken JJ, Graham TE, Heikkila JJ, &, Bonen A, (2008) Modest PGC-1alpha overexpression in muscle in vivo is sufficient to increase insulin sensitivity and palmitate oxidation in subsarcolemmal, not intermyofibrillar, mitochondria. J Biol Chem 283, 4228-4240.
150. Chomentowski P, Coen PM, Radikova Z, Goodpaster BH, &, Toledo FG, (2011) Skeletal muscle mitochondria in insulin resistance: differences in intermyofibrillar versus subsarcolemmal subpopulations and relationship to metabolic flexibility. J Clin Endocrinol Metab 96, 494-503.
151. Holloway GP, Gurd BJ, Snook LA, Lally J, &, Bonen A, (2010) Compensatory increases in nuclear PGC1alpha protein are primarily associated with subsarcolemmal mitochondrial adaptations in ZDF rats. Diabetes 59, 819-828.
152. Dyck DJ, Peters SJ, Glatz J, Gorski J, Keizer H, Kiens B, Liu S, Richter EA, Spriet LL, van der Vusse GJ, et al,. (1997) Functional differences in lipid metabolism in resting skeletal muscle of various fiber types. Am J Physiol 272, E340-E351.
153. Anderson EJ, Yamazaki H, &, Neufer PD, (2007) Induction of endogenous uncoupling protein 3 suppresses mitochondrial oxidant emission during fatty acid-supported respiration. J Biol Chem 282, 31257-31266.
154. Vincent AM, Edwards JL, McLean LL, Hong Y, Cerri F, Lopez I, Quattrini A, &, Feldman EL, (2010) Mitochondrial biogenesis and fission in axons in cell culture and animal models of diabetic neuropathy. Acta Neuropathol 120, 477-489.
155. Edwards JL, Quattrini A, Lentz SI, Figueroa-Romero C, Cerri F, Backus C, Hong Y, &, Feldman EL, (2010) Diabetes regulates mitochondrial biogenesis and fission in mouse neurons. Diabetologia 53, 160-169.
156. Jheng HF, Tsai PJ, Guo SM, Kuo LH, Chang CS, Su IJ, Chang CR, &, Tsai YS, (2012) Mitochondrial fission contributes to mitochondrial dysfunction and insulin resistance in skeletal muscle. Mol Cell Biol 32, 309-319.
157. Bach D, Pich S, Soriano FX, Vega N, Baumgartner B, Oriola J, Daugaard JR, Lloberas J, Camps M, Zierath JR, et al,. (2003) Mitofusin-2 determines
158. Joseph AM, Joanisse DR, Baillot RG, &, Hood DA, (2012) Mitochondrial dysregulation in the pathogenesis of diabetes: potential for mitochondrial biogenesis-mediated interventions. Exp Diabetes Res 2012, 642038.
159. Toledo FG, Watkins S, &, Kelley DE, (2006) Changes induced by physical activity and weight loss in the morphology of intermyofibrillar mitochondria in obese men and women. J Clin Endocrinol Metab 91, 3224-3227.
160. Menshikova EV, Ritov VB, Ferrell RE, Azuma K, Goodpaster BH, &, Kelley DE, (2007) Characteristics of skeletal muscle mitochondrial biogenesis induced by moderate-intensity exercise and weight loss in obesity. J Appl Physiol 103, 21-27.
161. Menshikova EV, Ritov VB, Toledo FG, Ferrell RE, Goodpaster BH, &, Kelley DE, (2005) Effects of weight loss and physical activity on skeletal muscle mitochondrial function in obesity. Am J Physiol Endocrinol Metab 288, E818-E825.
162. Goodpaster BH, Katsiaras A, &, Kelley DE, (2003) Enhanced fat oxidation through physical activity is associated with improvements in insulin sensitivity in obesity. Diabetes 52, 2191-2197.
163. Toledo FG, Menshikova EV, Ritov VB, Azuma K, Radikova Z, DeLany J, &, Kelley DE, (2007) Effects of physical activity and weight loss on skeletal muscle mitochondria and relationship with glucose control in type 2 diabetes. Diabetes 56, 2142-2147.
164. Wright DC, Han DH, Garcia-Roves PM, Geiger PC, Jones TE, &, Holloszy JO, (2007) Exercise-induced mitochondrial biogenesis begins before the increase in muscle PGC-1alpha expression. J Biol Chem 282, 194-199.
165. Holloszy JO, (1967) Biochemical adaptations in muscle. Effects of exercise on mitochondrial oxygen uptake and respiratory enzyme activity in skeletal muscle. J Biol Chem 242, 2278-2282.
166. Talanian JL, Galloway SD, Heigenhauser GJ, Bonen A, &, Spriet LL, (2007) Two weeks of high-intensity aerobic interval training increases the capacity for fat oxidation during exercise in women. J Appl Physiol 102, 1439-1447.
167. Bruce CR, Thrush AB, Mertz VA, Bezaire V, Chabowski A, Heigenhauser GJ, &, Dyck DJ, (2006) 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.
168. Amati F, Dube JJ, Shay C, &, Goodpaster BH, (2008) Separate and combined effects of exercise training and weight loss on exercise efficiency and substrate oxidation. J Appl Physiol 105, 825-831.
169. Toledo FG, Menshikova EV, Azuma K, Radikova Z, Kelley CA, Ritov VB, &, Kelley DE, (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, 987-994.
170. Bond DS, Phelan S, Leahey TM, Hill JO, &, Wing RR, (2009) Weight-loss maintenance in successful weight losers: surgical vs non-surgical methods. Int J Obes (Lond) 33, 173-180.
171. Catenacci VA, Ogden LG, Stuht J, Phelan S, Wing RR, Hill JO, &, Wyatt HR, (2008) Physical activity patterns in the National Weight Control Registry. Obesity (Silver Spring) 16, 153-161.
172. Goodpaster BH, (2013) Mitochondrial deficiency is associated with insulin resistance. Diabetes 62, 1032-1035.
173. Holloszy JO, (2013) 'Deficiency' of mitochondria in muscle does not cause insulin resistance. Diabetes 62, 1036-1040.