Normal mitochondrial function and increased fat oxidation capacity in leg and arm muscles in obese humans

International Journal of Obesity

Volumn 35, Issue 1, 2011, Pages 99-108

  Ara, I ^a,b,c   Larsen, S ^c   Stallknecht, B ^c   Guerra, B ^d   Morales Alamo, D ^d   Andersen, J L ^e   Ponce Gonzalez J G ^d   Guadalupe Grau, A ^d   Galbo, H ^c   Calbet, J A L ^d   Helge, J W ^c  

^a UNIVERSITY OF CASTILLA LA MANCHA   (Spain)

^b UNIVERSITY OF ZARAGOZA   (Spain)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d UNIVERSITY OF LAS PALMAS DE GRAN CANARIA   (Spain)

^e BISPEBJERG HOSPITAL   (Denmark)

Author keywords

adiponectin; lipid oxidation; physical activity; weight loss

Indexed keywords

ADIPONECTIN; CARBOHYDRATE; FAT; FATTY ACID; LEPTIN; MUSCLE ENZYME; SAPONIN;

ADULT; ARM MUSCLE; ARTICLE; BODY MASS; CALORIMETRY; CLINICAL ARTICLE; CONTROLLED STUDY; DELTOID MUSCLE; ENZYME ACTIVITY; EXERCISE INTENSITY; EXERCISE TEST; HUMAN; HUMAN TISSUE; HYPOTHESIS; LEG EXERCISE; LEG MUSCLE; MALE; MITOCHONDRIAL RESPIRATION; MUSCLE BIOPSY; OBESITY; OXIDATION; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; RESPIROMETRY; TRIACYLGLYCEROL BLOOD LEVEL; VASTUS LATERALIS MUSCLE; WEIGHT REDUCTION; WORKLOAD;

ADIPONECTIN; ADULT; AGE DISTRIBUTION; ARM; BLOTTING, WESTERN; BODY MASS INDEX; CALORIMETRY, INDIRECT; ENERGY METABOLISM; EXERCISE TEST; FATTY ACIDS, NONESTERIFIED; HUMANS; LEG; LIPID METABOLISM; MALE; MITOCHONDRIA; MUSCLE, SKELETAL; OBESITY; OXIDATION-REDUCTION; PROSPECTIVE STUDIES; QUESTIONNAIRES; TRIGLYCERIDES;

EID: 78651295010     PISSN: 03070565     EISSN: 14765497     Source Type: Journal    
DOI: 10.1038/ijo.2010.123     Document Type: Article

References (57)

1. Holloszy JO, Kohrt WM, Hansen PA. The regulation of carbohydrate and fat metabolism during and after exercise. Front Biosci 1998; 3: D1011-D1027.
2. Kelley DE, Goodpaster B, Wing RR, Simoneau JA. Skeletal muscle fatty acid metabolism in association with insulin resistance, obesity, and weight loss. Am J Physiol 1999; 277 (6 Part 1): E1130-E1141.
3. Kim JY, Hickner RC, Cortright RL, Dohm GL, Houmard JA. Lipid oxidation is reduced in obese human skeletal muscle. Am J Physiol Endocrinol 2000; 279: E1039-E1044.
4. Perez-Martin A, Dumortier M, Raynaud E, Brun JF, Fedou C, Bringer J et al. Balance of substrate oxidation during submaximal exercise in lean and obese people. Diabetes Metab 2001; 27 (4 Part 1): 466-474.
5. Simoneau JA, Veerkamp JH, Turcotte LP, Kelley DE. Markers of capacity to utilize fatty acids in human skeletal muscle: relation to insulin resistance and obesity and effects of weight loss. FASEB J 1999; 13: 2051-2060.
6. Thyfault JP, Kraus RM, Hickner RC, Howell AW, Wolfe RR, Dohm GL. Impaired plasma fatty acid oxidation in extremely obese women. Am J Physiol Endocrinol Metab 2004; 287: E1076-E1081.
7. Goodpaster BH, Wolfe RR, Kelley DE. Effects of obesity on substrate utilization during exercise. Obes Res 2002; 10: 575-584.
8. Kanaley JA, Cryer PE, Jensen MD. Fatty acid kinetic responses to exercise. Effects of obesity, body fat distribution, and energy-restricted diet. J Clin Invest 1993; 92: 255-261.
9. Fuentes T, Ara I, Guadalupe-Grau A, Larsen S, Stallknecht B, Olmedillas H et al. Leptin receptor 170 KDa (OB-R170) protein expression is reduced in obese human skeletal muscle: a potential mechanism of leptin resistance. Exp Physiol 2010; 95: 160-171.
10. Hojlund K, Mogensen M, Sahlin K, Beck-Nielsen H. Mitochon-drial dysfunction in type 2 diabetes and obesity. Endocrinol Metab Clin North Am 2008; 37: 713-731, x.
11. Kelley DE, He J, Menshikova EV, Ritov VB. Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 2002; 51: 2944-2950.
12. Mogensen M, Sahlin K, Fernstrom M, Glintborg D, Vind BF, Beck-Nielsen H et al. Mitochondrial respiration is decreased in skeletal muscle of patients with type 2 diabetes. Diabetes 2007; 56: 1592-1599.
13. Larsen S, Ara I, Rabol R, Andersen JL, Boushel R, Dela F et al. Are substrate use during exercise and mitochondrial respiratory capacity decreased in arm and leg muscle in type 2 diabetes? Diabetologia 2009; 52: 1400-1408.
14. Menshikova EV, Ritov VB, Toledo FG, Ferrell RE, Goodpaster BH, Kelley DE. Effects of weight loss and physical activity on skeletal muscle mitochondrial function in obesity. Am J Physiol Endocrinol Metab 2005; 288: E818-E825.
15. Greco AV, Mingrone G, Giancaterini A, Manco M, Morroni M, Cinti S et al. Insulin resistance in morbid obesity: reversal with intramyocellular fat depletion. Diabetes 2002; 51: 144-151.
16. Kempen KP, Saris WH, Kuipers H, Glatz JF, Van DV. Skeletal muscle metabolic characteristics before and after energy restriction in human obesity: fibre type, enzymatic beta-oxidative capacity and fatty acid-binding protein content. Eur J Clin Invest 1998; 28: 1030-1037.
17. Raben A, Mygind E, Astrup A. Lower activity of oxidative key enzymes and smaller fiber areas in skeletal muscle of postobese women. Am J Physiol Endocrinol 1998; 38: E487-E494.
18. Olsen DB, Sacchetti M, Dela F, Ploug T, Saltin B. Glucose clearance is higher in arm than leg muscle in type 2 diabetes. J Physiol 2005; 565 (Part 2): 555-562.
19. Reynolds TH, Supiano MA, Dengel DR. Regional differences in glucose clearance: effects of insulin and resistance training on arm and leg glucose clearance in older hypertensive individuals. J Appl Physiol 2007; 102: 985-991.
20. Sacchetti M, Olsen DB, Saltin B, van Hall G. Heterogeneity in limb fatty acid kinetics in type 2 diabetes. Diabetologia 2005; 48: 938-945.
21. Bergström J. Muscle electrolytes in man: determined by neutron activation analysis on needle biopsy specimens. A study on normal subjects, kidney patients and patients with chronic diarrhea. Scand J Clin Lab Invest 1962; 68 (Supplementum): 11-13.
22. Achten J, Gleeson M, Jeukendrup AE. Determination of the exercise intensity that elicits maximal fat oxidation. Med Sci Sports Exerc 2002; 34: 92-97.
23. Washburn RA, Seals DR. Comparison of peak oxygen uptake in arm cranking. Eur J Appl Physiol Occup Physiol 1983; 51: 3-6.
24. Smith PM, Doherty M, Price MJ. The effect of crank rate on physiological responses and exercise efficiency using a range of submaximal workloads during arm crank ergometry. Int J Sports Med 2006; 27: 199-204.
25. Kuznetsov AV, Veksler V, Gellerich FN, Saks V, Margreiter R, Kunz W S. Analysis of mitochondrial function in situ in permeabilized muscle fibers, tissues and cells. Nat Protoc 2008; 3: 965-976.
26. Brooke MH, Kaiser KK. Three 'myosin ATPase' systems: the nature of their pH lability and sulfhydryl dependence. J Histochem Cytochem 1970; 18: 670-672.
27. Qu Z, Andersen JL, Zhou S. Visualisation of capillaries in human skeletal muscle. Histochem Cell Biol 1997; 107: 169-174.
28. Andersen JL, Aagaard P. Myosin heavy chain IIX overshoot in human skeletal muscle. Muscle Nerve 2000; 23: 1095-1104.
29. Andersen JL, Schjerling P, Andersen LL, Dela F. Resistance training and insulin action in humans: effects of de-training. J Physiol 2003; 551 (Part 3): 1049-1058.
30. Langfort J, Ploug T, Ihlemann J, Baranczuk E, Donsmark M, Gorski J et al. Additivity of adrenaline and contractions on hormone-sensitive lipase, but not on glycogen phosphorylase, in rat muscle. Acta Physiol Scand 2003; 178: 51-60.
31. Helge JW, Dela F. Effect of training on muscle triacylglycerol and structural lipids: a relation to insulin sensitivity? Diabetes 2003; 52: 1881-1887.
32. Guerra B, Santana A, Fuentes T, gado-Guerra S, Cabrera-Socorro A, Dorado C et al. Leptin receptors in human skeletal muscle. J Appl Physiol 2007; 102: 1786-1792.
33. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD et al. Measurement of protein using bicincho-ninic acid. Anal Biochem 1985; 150: 76-85.
34. Towbin H, Staehelin T, Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. 1979. Biotechnology 1992; 24: 145-149.
35. Frayn K. Calculation of substrate oxidation rates in vivo from gaseous exchange. J Appl Physiol 1983; 55: 628-634.
36. Weir JB. New methods for calculating metabolic rate with special reference to protein metabolism. J Physiol 1949; 109: 1-9.
37. Mogensen M, Bagger M, Pedersen PK, Fernstrom M, Sahlin K. Cycling efficiency in humans is related to low UCP3 content and to type I fibres but not to mitochondrial efficiency. J Physiol 2006; 571 (Part 3): 669-681.
38. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 1985; 28: 412-419.
39. Craig CL, Marshall AL, Sjostrom M, Bauman AE, Booth ML, Ainsworth BE et al. International physical activity questionnaire: 12-country reliability and validity. Med Sci Sports Exerc 2003; 35: 1381-1395.
40. Holloszy JO, Coyle EF. Adaptations of skeletal muscle to endurance exercise and their metabolic consequences. J Appl Physiol 1984; 56: 831-838.
41. Turcotte LP, Richter EA, Kiens B. Increased plasma FFA uptake and oxidation during prolonged exercise in trained vs untrained humans. Am J Physiol 1992; 262: E791-E799.
42. Horowitz JF, Klein S. Oxidation of nonplasma fatty acids during exercise is increased in women with abdominal obesity. J Appl Physiol 2000; 89: 2276-2282.
43. Alsted TJ, Nybo L, Schweiger M, Fledelius C, Jacobsen P, Zimmermann R et al. Adipose triglyceride lipase in human skeletal muscle is upregulated by exercise training. Am J Physiol Endocrinol Metab 2009; 296: E445-E453.
44. McGarry JD, Mills SE, Long CS, Foster DW. Observations on the affinity for carnitine, and malonyl-CoA sensitivity, of carnitine palmitoyltransferase I in animal and human tissues. Demonstration of the presence of malonyl-CoA in non-hepatic tissues of the rat. Biochem J 1983; 214: 21-28.
45. Yamauchi T, Kamon J, Minokoshi Y, Ito Y, Waki H, Uchida S et al. Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase. Nat Med 2002; 8: 1288-1295.
46. Saha AK, Schwarsin AJ, Roduit R, Masse F, Kaushik V, Tornheim K et al. Activation of malonyl CoA decarboxylase in rat skeletal muscle by contraction and the AMP-activated protein kinase activator AICAR. J Biol Chem 2000; 32: 24279-24283.
47. Jurimae J, Kums T, Jurimae T. Plasma adiponectin concentration is associated with the average accelerometer daily steps counts in healthy elderly females. Eur J Appl Physiol 2010, e-pub ahead of print 13 March 2010.
48. Ring-Dimitriou S, Paulweber B, von Duvillard SP, Stadlmann M, LeMura LM, Lang J et al. The effect of physical activity and physical fitness on plasma adiponectin in adults with predisposition to metabolic syndrome. Eur J Appl Physiol 2006; 98: 472-481.
49. Löfgren P, Andersson I, Adolfsson B, Leijonhufvud BM, Hertel K, Hoffstedt J et al. Long-term prospective and controlled studies demonstrate adipose tissue hypercellularity and relative leptin deficiency in the postobese state. Clin Endocrinol Metab 2005; 11: 6207-6213.
50. Muoio DM, Dohn GL, Fiedorek FT, Tapscott EB, Coleman RA. Leptin directly alters lipid partitioning in skeletal muscle. Diabetes 1997; 46: 1360-1363.
51. Steinberg GR, Parolin ML, Heigenhauser GJ, Dyck DJ. Leptin increases FA oxidation in lean but not obese human skeletal muscle: evidence of peripheral leptin resistance. Am J Physiol Endocrinol Metab 2002; 283: E187-E192.
52. Bjorbaek C, El-Haschimi K, Frantz JD, Flier JS. The role of SOCS-3 in leptin signaling and leptin resistance. J Biol Chem 1999; 274: 30059-30065.
53. Steinberg GR, McAinch AJ, Chen MB, O'Brien PE, Dixon JB, Cameron-Smith D et al. The suppressor of cytokine signaling 3inhibits leptin activation of AMP-kinase in cultured skeletal muscle of obese humans. J Clin Endocrinol Metab 2006; 91: 3592-3597.
54. Houmard JA. Do the mitochondria of obese individuals respond to exercise training? J Appl Physiol 2007; 103: 6-7.
55. Menshikova EV, Ritov VB, Ferrell RE, Azuma K, Goodpaster BH, Kelley DE. Characteristics of skeletal muscle mitochondrial biogenesis induced by moderate-intensity exercise and weight loss in obesity. J Appl Physiol 2007; 103: 21-27.
56. Ritov VB, Menshikova EV, He J, Ferrell RE, Goodpaster BH, Kelley DE. Deficiency of subsarcolemmal mitochondria in obesity and type 2 diabetes. Diabetes 2005; 54: 8-14.
57. Rabol R, Svendsen PF, Skovbro M, Boushel R, Haugaard SB, Schjerling P et al. 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 2009; 58: 1145-1152.