Impaired protein metabolism: Interlinks between obesity, insulin resistance and inflammation

Obesity Reviews

Volumn 13, Issue SUPPL.2, 2012, Pages 51-57

  Guillet, C ^a,b,c   Masgrau, A ^a,b,c   Walrand, S ^a,b,c   Boirie, Y ^a,b,c  

^a UNIVERSITÉ CLERMONT AUVERGNE   (France)

^b INRA and University of Auvergne   (France)

^c UNIVERSITY HOSPITAL OF CLERMONT FERRAND   (France)

Author keywords

Insulin; Lipids; Obesity; Skeletal muscle

Indexed keywords

3 HYDROXYACYL COENZYME A DEHYDROGENASE; C REACTIVE PROTEIN; CARNITINE PALMITOYLTRANSFERASE I; CITRATE SYNTHASE; FATTY ACID; INSULIN; INTERLEUKIN 6; LEPTIN; LEPTIN RECEPTOR; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; BODY FAT DISTRIBUTION; DISEASE COURSE; DISORDERS OF LIPID AND LIPOPROTEIN METABOLISM; ENZYME ACTIVITY; HUMAN; HYPERINSULINEMIA; INFLAMMATION; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; INSULIN SENSITIVITY; LEAN BODY WEIGHT; LIPID OXIDATION; LIPID STORAGE; LIPOLYSIS; MUSCLE MASS; MUSCLE STRENGTH; NONHUMAN; OBESITY; OXIDATIVE STRESS; PHENOTYPE; PROTEIN DEGRADATION; PROTEIN METABOLISM; PROTEIN SYNTHESIS; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; WEIGHT GAIN;

ADIPOSE TISSUE; BODY COMPOSITION; HUMANS; INFLAMMATION; INSULIN RESISTANCE; LIPID METABOLISM; MUSCLE PROTEINS; MUSCLE STRENGTH; MUSCLE, SKELETAL; OBESITY; OXIDATION-REDUCTION;

EID: 84868132234     PISSN: 14677881     EISSN: 1467789X     Source Type: Journal    
DOI: 10.1111/j.1467-789X.2012.01037.x     Document Type: Article

References (87)

1. Bray GA. Medical consequences of obesity. J Clin Endocrinol Metab 2004; 89: 2583-2589.
2. Gray SL, Vidal-Puig AJ. Adipose tissue expandability in the maintenance of metabolic homeostasis. Nutr Rev 2007; 65: S7-S12.
3. Slawik M, Vidal-Puig AJ. Adipose tissue expandability and the metabolic syndrome. Genes Nutr 2007; 2: 41-45.
4. Krssak M, Falk Petersen K, Dresner A etal. Intramyocellular lipid concentrations are correlated with insulin sensitivity in humans: a 1H NMR spectroscopy study. Diabetologia 1999; 42: 113-116.
5. Perseghin G, Scifo P, De Cobelli F etal. Intramyocellular triglyceride content is a determinant of in vivo insulin resistance in humans: a 1H-13C nuclear magnetic resonance spectroscopy assessment in offspring of type 2 diabetic parents. Diabetes 1999; 48: 1600-1606.
6. Virkamaki A, Korsheninnikova E, Seppala-Lindroos A etal. Intramyocellular lipid is associated with resistance to in vivo insulin actions on glucose uptake, antilipolysis, and early insulin signaling pathways in human skeletal muscle. Diabetes 2001; 50: 2337-2343.
7. Houmard JA, Pories WJ, Dohm GL. Is there a metabolic program in the skeletal muscle of obese individuals? J Obes 2011; Epub 26 April 2011.
8. Forbes GB, Welle SL. Lean body mass in obesity. Int J Obes 1983; 7: 99-107.
9. Lafortuna CL, Maffiuletti NA, Agosti F, Sartorio A. Gender variations of body composition, muscle strength and power output in morbid obesity. Int J Obes (Lond) 2005; 29: 833-841.
10. Webster JD, Hesp R, Garrow JS. The composition of excess weight in obese women estimated by body density, total body water and total body potassium. Hum Nutr Clin Nutr 1984; 38: 299-306.
11. Durschlag RP, Layman DK. Skeletal muscle growth in lean and obese Zucker rats. Growth 1983; 47: 282-291.
12. Fluckey JD, Pohnert SC, Boyd SG, Cortright RN, Trappe TA, Dohm GL. Insulin stimulation of muscle protein synthesis in obese Zucker rats is not via a rapamycin-sensitive pathway. Am J Physiol Endocrinol Metab 2000; 279: E182-E187.
13. Kemp JG, Blazev R, Stephenson DG, Stephenson GM. Morphological and biochemical alterations of skeletal muscles from the genetically obese (ob/ob) mouse. Int J Obes (Lond) 2009; 33: 831-841.
14. Adéchian S, Giardina S, Rémond D etal. Excessive energy intake does not modify fed-state tissue protein synthesis rates in adult rats. Obesity (Silver Spring) 2009; 17: 1348-1355.
15. Borst SE, Conover CF. High-fat diet induces increased tissue expression of TNF-alpha. Life Sci 2005; 77: 2156-2165.
16. Chanseaume E, Giraudet C, Gryson C etal. Enhanced muscle mixed and mitochondrial protein synthesis rates after a high-fat or high-sucrose diet. Obesity (Silver Spring) 2007; 15: 853-859.
17. Janssen I, Heymsfield SB, Wang ZM, Ross R. Skeletal muscle mass and distribution in 468 men and women aged 18-88yr. J Appl Physiol 2000; 89: 81-88.
18. Lillioja S, Young AA, Culter CL etal. Skeletal muscle capillary density and fiber type are possible determinants of in vivo insulin resistance in man. J Clin Invest 1987; 80: 415-424.
19. Tanner CJ, Barakat HA, Dohm GL etal. Muscle fiber type is associated with obesity and weight loss. Am J Physiol Endocrinol Metab 2002; 282: E1191-E1196.
20. Simoneau JA, Colberg SR, Thaete FL, Kelley DE. Skeletal muscle glycolytic and oxidative enzyme capacities are determinants of insulin sensitivity and muscle composition in obese women. FASEB J 1995; 9: 273-278.
21. Katsanos CS, Aarsland A, Cree MG, Wolfe RR. Muscle protein synthesis and balance responsiveness to essential amino acids ingestion in the presence of elevated plasma free fatty acid concentrations. J Clin Endocrinol Metab 2009; 94: 2984-2990.
22. Hickey MS, Carey JO, Azevedo JL etal. Skeletal muscle fiber composition is related to adiposity and in vitro glucose transport rate in humans. Am J Physiol 1995; 268: E453-E457.
23. Must A, Spadano J, Coakley EH, Field AE, Colditz G, Dietz WH. The disease burden associated with overweight and obesity. JAMA 1999; 282: 1523-1529.
24. Holmäng A, Brzezinska Z, Björntorp P. Effects of hyperinsulinemia on muscle fiber composition and capitalization in rats. Diabetes 1993; 42: 1073-1081.
25. Helge JW, Fraser AM, Kriketos AD etal. Interrelationships between muscle fibre type, substrate oxidation and body fat. Int J Obes Relat Metab Disord 1999; 23: 986-991.
26. Wade AJ, Marbut MM, Round JM. Muscle fibre type and aetiology of obesity. Lancet 1990; 335: 805-808.
27. He J, Watkins S, Kelley DE. Skeletal muscle lipid content and oxidative enzyme activity in relation to muscle fiber type in type 2 diabetes and obesity. Diabetes 2001; 50: 817-823.
28. Kempen KP, Saris WH, Kuipers H, Glatz JF, Van Der Vusse GJ. 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.
29. Abou Mrad J, Yakubu F, Lin D, Peters JC, Atkinson JB, Hill JO. Skeletal muscle composition in dietary obesity-susceptible and dietary obesity-resistant rats. Am J Physiol 1992; 262: R684-R688.
30. Zurlo F, Lillioja S, Esposito-Del Puente A etal. Low ratio of fat to carbohydrate oxidation as predictor of weight gain: study of 24-h RQ. Am J Physiol 1990; 259: E650-E657.
31. Goodpaster BH, Theriault R, Watkins SC, Kelley DE. Intramuscular lipid content is increased in obesity and decreased by weight loss. Metabolism 2000; 49: 467-472.
32. Kelley DE, Slasky BS, Janosky J. Skeletal muscle density: effects of obesity and non-insulin-dependent diabetes mellitus. Am J Clin Nutr 1991; 54: 509-515.
33. 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: E1130-E1141.
34. Goodpaster BH, Thaete FL, Kelley DE. Thigh adipose tissue distribution is associated with insulin resistance in obesity and in type 2 diabetes mellitus. Am J Clin Nutr 2000; 71: 885-892.
35. Mazzali G, Di Francesco V, Zoico E etal. Interrelations between fat distribution, muscle lipid content, adipocytokines, and insulin resistance: effect of moderate weight loss in older women. Am J Clin Nutr 2006; 84: 1193-1199.
36. Pan DA, Lillioja S, Kriketos AD etal. Skeletal muscle triglyceride levels are inversely related to insulin action. Diabetes 1997; 46: 983-988.
37. Kim JY, Hickner RC, Cortright RL, Dohm GL, Houmard JA. Lipid oxidation is reduced in obese human skeletal muscle. Am J Physiol Endocrinol Metab 2000; 279: E1039-E1044.
38. Hulens M, Vansant G, Lysens R, Claessens AL, Muls E, Brumagne S. Study of differences in peripheral muscle strength of lean versus obese women: an allometric approach. Int J Obes Relat Metab Disord 2001; 25: 676-681.
39. Maffiuletti NA, Jubeau M, Munzinger U etal. Differences in quadriceps muscle strength and fatigue between lean and obese subjects. Eur J Appl Physiol 2007; 101: 51-59.
40. Pescatello LS, Kelsey BK, Price TB etal. The muscle strength and size response to upper arm, unilateral resistance training among adults who are overweight and obese. J Strength Cond Res 2007; 21: 307-313.
41. Kitagawa K, Miyashita M. Muscle strengths in relation to fat storage rate in young men. Eur J Appl Physiol Occup Physiol 1978; 38: 189-196.
42. Duvigneaud N, Matton L, Wijndaele K etal. Relationship of obesity with physical activity, aerobic fitness and muscle strength in Flemish adults. J Sports Med Phys Fitness 2008; 48: 201-210.
43. Stenholm S, Sallinen J, Koster A etal. Association between obesity history and hand grip strength in older adults - exploring the roles of inflammation and insulin resistance as mediating factors. J Gerontol A Biol Sci Med Sci 2011; 66: 341-348.
44. Delmonico MJ, Harris TB, Visser M etal. Longitudinal study of muscle strength, quality, and adipose tissue infiltration. Am J Clin Nutr 2009; 90: 1579-1585.
45. Visser M, Kritchevsky SB, Goodpaster BH etal. Leg muscle mass and composition in relation to lower extremity performance in men and women aged 70 to 79: the health, aging and body composition study. J Am Geriatr Soc 2002; 50: 897-904.
46. Hilton TN, Tuttle LJ, Bohnert KL, Mueller MJ, Sinacore DR. Excessive adipose tissue infiltration in skeletal muscle in individuals with obesity, diabetes mellitus, and peripheral neuropathy: association with performance and function. Phys Ther 2008; 88: 1336-1344.
47. Bergen WG. Protein synthesis in animal models. J Anim Sci 1974; 38: 1079-1091.
48. Chan CP, Koong LJ, Stern JS. Effect of insulin on fat and protein deposition in diabetic lean and obese rats. Am J Physiol 1982; 242: E19-E24.
49. Stolz DJ, Martin RJ. Role of insulin in food intake, weight gain and lipid deposition in the Zucker obese rat. J Nutr 1982; 112: 997-1002.
50. Masgrau A, Mishellany-Dutour A, Murakami H etal. Time-course changes of muscle protein synthesis associated with obesity-induced lipotoxicity. J Physiol 2012; [Epub ahead of print].
51. Kahn BB, Flier JS. Obesity and insulin resistance. J Clin Invest 2000; 106: 473-481.
52. Biolo G, Wolfe RR. Insulin action on protein metabolism. Baillieres Clin Endocrinol Metab 1993; 7: 989-1005.
53. Castellino P, Luzi L, Simonson DC, Haymond M, DeFronzo RA. Effect of insulin and plasma amino acid concentrations on leucine metabolism in man. Role of substrate availability on estimates of whole body protein synthesis. J Clin Invest 1987; 80: 1784-1793.
54. Meek SE, Persson M, Ford GC, Nair KS. Differential regulation of amino acid exchange and protein dynamics across splanchnic and skeletal muscle beds by insulin in healthy human subjects. Diabetes 1998; 47: 1824-1835.
55. Guillet C, Delcourt I, Rance M etal. Changes in basal and insulin and amino acid response of whole body and skeletal muscle proteins in obese men. J Clin Endocrinol Metab 2009; 94: 3044-3050.
56. Guillet C, Prod'homme M, Balage M etal. Impaired anabolic response of muscle protein synthesis is associated with S6K1 dysregulation in elderly humans. FASEB J 2004; 18: 1586-1587.
57. Guillet C, Zangarelli A, Gachon P etal. Whole body protein breakdown is less inhibited by insulin, but still responsive to amino acid, in nondiabetic elderly subjects. J Clin Endocrinol Metab 2004; 89: 6017-6024.
58. Halvatsiotis PG, Turk D, Alzaid A, Dinneen S, Rizza RA, Nair KS. Insulin effect on leucine kinetics in type 2 diabetes mellitus. Diabetes Nutr Metab 2002; 15: 136-142.
59. Luzi L, Castellino P, DeFronzo RA. Insulin and hyperaminoacidemia regulate by a different mechanism leucine turnover and oxidation in obesity. Am J Physiol 1996; 270: E273-E281.
60. Caballero B, Wurtman RJ. Differential effects of insulin resistance on leucine and glucose kinetics in obesity. Metabolism 1991; 40: 51-58.
61. Welle S, Statt M, Barnard R, Amatruda J. Differential effect of insulin on whole-body proteolysis and glucose metabolism in normal-weight, obese, and reduced-obese women. Metabolism 1994; 43: 441-445.
62. Chevalier S, Marliss EB, Morais JA, Lamarche M, Gougeon R. Whole-body protein anabolic response is resistant to the action of insulin in obese women. Am J Clin Nutr 2005; 82: 355-365.
63. Felig P, Marliss E, Cahill GF Jr. Plasma amino acid levels and insulin secretion in obesity. N Engl J Med 1969; 281: 811-816.
64. She P, Van Horn C, Reid T, Hutson SM, Cooney RN, Lynch CJ. Obesity-related elevations in plasma leucine are associated with alterations in enzymes involved in branched-chain amino acid metabolism. Am J Physiol Endocrinol Metab 2007; 293: E1552-E1563.
65. Wang TJ, Larson MG, Vasan RS etal. Metabolite profiles and the risk of developing diabetes. Nat Med 2011; 17: 448-453.
66. Anderson SR, Gilge DA, Steiber AL, Previs SF. Diet-induced obesity alters protein synthesis: tissue-specific effects in fasted versus fed mice. Metabolism 2008; 57: 347-354.
67. Chan CP, Hansen RJ, Stern JS. Protein turnover in insulin-treated, alloxan-diabetic lean and obese Zucker rats. J Nutr 1985; 115: 959-969.
68. Shargill NS, Ohshima K, Bray GA, Chan TM. Muscle protein turnover in the perfused hindquarters of lean and genetically obese-diabetic (db/db) mice. Diabetes 1984; 33: 1160-1164.
69. Jensen MD, Haymond MW. Protein metabolism in obesity: effects of body fat distribution and hyperinsulinemia on leucine turnover. Am J Clin Nutr 1991; 53: 172-176.
70. Solini A, Bonora E, Bonadonna R, Castellino P, DeFronzo RA. Protein metabolism in human obesity: relationship with glucose and lipid metabolism and with visceral adipose tissue. J Clin Endocrinol Metab 1997; 82: 2552-2558.
71. Lang CH. Elevated plasma free fatty acids decrease basal protein synthesis, but not the anabolic effect of leucine, in skeletal muscle. Am J Physiol Endocrinol Metab 2006; 291: E666-E674.
72. Fery F, Plat L, Baleriaux M, Balasse EO. Inhibition of lipolysis stimulates whole body glucose production and disposal in normal postabsorptive subjects. J Clin Endocrinol Metab 1997; 82: 825-830.
73. Jeejeebhoy KN, Anderson GH, Nakhooda AF, Greenberg GR, Sanderson I, Marliss EB. Metabolic studies in total parenteral nutrition with lipid in man. Comparison with glucose. J Clin Invest 1976; 57: 125-136.
74. Tessari P, Nissen SL, Miles JM, Haymond MW. Inverse relationship of leucine flux and oxidation to free fatty acid availability in vivo. J Clin Invest 1986; 77: 575-581.
75. Samuel VT, Petersen KF, Shulman GI. Lipid-induced insulin resistance: unravelling the mechanism. Lancet 2010; 375: 2267-2277.
76. Nguyen XM, Lane J, Smith BR, Nguyen NT. Changes in inflammatory biomarkers across weight classes in a representative US population: a link between obesity and inflammation. J Gastrointest Surg 2009; 13: 1205-1212.
77. Marette A. Mediators of cytokine-induced insulin resistance in obesity and other inflammatory settings. Curr Opin Clin Nutr Metab Care 2002; 5: 377-383.
78. Xu H, Barnes GT, Yang Q etal. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 2003; 112: 1821-1830.
79. Goodman MN. Tumor necrosis factor induces skeletal muscle protein breakdown in rats. Am J Physiol 1991; 260: E727-E730.
80. Goodman MN. Interleukin-6 induces skeletal muscle protein breakdown in rats. Proc Soc Exp Biol Med 1994; 205: 182-185.
81. Balage M, Averous J, Remond D etal. Presence of low-grade inflammation impaired postprandial stimulation of muscle protein synthesis in old rats. J Nutr Biochem 2010; 21: 325-331.
82. Pasini E, Aquilani R, Dioguardi FS, D'Antona G, Gheorghiade M, Taegtmeyer H. Hypercatabolic syndrome: molecular basis and effects of nutritional supplements with amino acids. Am J Cardiol 2008; 101: 11E-15E.
83. Visser M, Pahor M, Taaffe DR etal. Relationship of interleukin-6 and tumor necrosis factor-alpha with muscle mass and muscle strength in elderly men and women: the Health ABC Study. J Gerontol A Biol Sci Med Sci 2002; 57: M326-M332.
84. Cesari M, Kritchevsky SB, Baumgartner RN etal. Sarcopenia, obesity, and inflammation- results from the trial of angiotensin converting enzyme inhibition and novel cardiovascular risk factors study. Am J Clin Nutr 2005; 82: 428-434.
85. Taaffe DR, Harris TB, Ferrucci L, Rowe J, Seeman TE. Cross-sectional and prospective relationships of interleukin-6 and C-reactive protein with physical performance in elderly persons: MacArthur studies of successful aging. J Gerontol A Biol Sci Med Sci 2000; 55: M709-M715.
86. Schrager MA, Metter EJ, Simonsick E etal. Sarcopenic obesity and inflammation in the InCHIANTI study. J Appl Physiol 2007; 102: 919-925.
87. Schaap LA, Pluijm SM, Deeg DJ, Visser M. Inflammatory markers and loss of muscle mass (sarcopenia) and strength. Am J Med 2006; 119: 526.e9-526.e17.