Time-course changes of muscle protein synthesis associated with obesity-induced lipotoxicity

Journal of Physiology

Volumn 590, Issue 20, 2012, Pages 5199-5210

  Masgrau, Aurélie ^a,b   Mishellany Dutour, Anne ^a,b   Murakami, Hitoshi ^a,b   Beaufrère, Anne Marie ^c   Walrand, Stéphane ^a,b   Giraudet, Christophe ^a,b   Migné, Carole ^a,b   Gerbaix, Maude ^b   Metz, Lore ^b   Courteix, Daniel ^b   Guillet, Christelle ^a,b   Boirie, Yves ^a,b,c  

^a CEMAGREF   (France)

^b UNIVERSITÉ CLERMONT AUVERGNE   (France)

^c UNIVERSITY HOSPITAL OF CLERMONT FERRAND   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA ACTIN; CARBON 13; LIPID; MUSCLE PROTEIN; VALINE;

ANALYTICAL PARAMETERS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTHROPOMETRIC PARAMETERS; ARTICLE; BODY COMPOSITION; CONTROLLED STUDY; DISEASE COURSE; DUAL ENERGY X RAY ABSORPTIOMETRY; FAT MASS; FRACTIONAL SYNTHESIS RATE; GLYCOLYSIS; HISTOCHEMISTRY; LIPID COMPOSITION; LIPID DIET; LIPID TRANSPORT; LIPOTOXICITY; MALE; MUSCLE MASS; MUSCLE MITOCHONDRION; NONHUMAN; OBESITY; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN SYNTHESIS INHIBITION; RAT; SKELETAL MUSCLE; SOLEUS MUSCLE; STEADY STATE; SUGAR INTAKE; TIBIALIS ANTERIOR MUSCLE; TISSUE STRUCTURE; WEIGHT GAIN;

EID: 84867478430     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2012.238576     Document Type: Article

References (71)

1. Adams JM 2nd, Pratipanawatr T, Berria R, Wang E, DeFronzo RA, Sullards MC & Mandarino LJ (2004). Ceramide content is increased in skeletal muscle from obese insulin-resistant humans. Diabetes 53, 25-31.
2. Adechian S, Giardina S, Remond D, Papet I, Buonocore D, Gaudichon C, Dardevet D, Marzatico F & Mosoni L (2009). Excessive energy intake does not modify fed-state tissue protein synthesis rates in adult rats. Obesity (Silver Spring) 17, 1348-1355.
3. Anderson SR, Gilge DA, Steiber AL & Previs SF (2008). Diet-induced obesity alters protein synthesis: tissue-specific effects in fasted versus fed mice. Metabolism 57, 347-354.
4. Argiles JM, Busquets S, Alvarez B & Lopez-Soriano FJ (1999). Mechanism for the increased skeletal muscle protein degradation in the obese Zucker rat. J Nutr Biochem 10, 244-248.
5. Bassel-Duby R & Olson EN (2006). Signaling pathways in skeletal muscle remodeling. Annu Rev Biochem 75, 19-37.
6. Bastard JP, Maachi M, Lagathu C, Kim MJ, Caron M, Vidal H, Capeau J & Feve B (2006). Recent advances in the relationship between obesity, inflammation, and insulin resistance. Eur Cytokine Netw 17, 4-12.
7. Benhizia F, Hainault I, Serougne C, Lagrange D, Hajduch E, Guichard C, Malewiak MI, Quignard-Boulange A, Lavau M & Griglio S (1994). Effects of a fish oil-lard diet on rat plasma lipoproteins, liver FAS, and lipolytic enzymes. Am J Physiol Endocrinol Metab 267, E975-E982.
8. Bodine SC, Stitt TN, Gonzalez M, Kline WO, Stover GL, Bauerlein R, Zlotchenko E, Scrimgeour A, Lawrence JC, Glass DJ & Yancopoulos GD (2001). Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol 3, 1014-1019.
9. Boirie Y, Short KR, Ahlman B, Charlton M & Nair KS (2001). Tissue-specific regulation of mitochondrial and cytoplasmic protein synthesis rates by insulin. Diabetes 50, 2652-2658.
10. Borst SE & Conover CF (2005). High-fat diet induces increased tissue expression of TNF-alpha. Life Sci 77, 2156-2165.
11. Bray GA (2004). Medical consequences of obesity. J Clin Endocrinol Metab 89, 2583-2589.
12. Carobbio S, Rodriguez-Cuenca S & Vidal-Puig A (2011). Origins of metabolic complications in obesity: ectopic fat accumulation. The importance of the qualitative aspect of lipotoxicity. Curr Opin Clin Nutr Metab Care 14, 520-526.
13. Castellino P, Luzi L, Simonson DC, Haymond M & DeFronzo RA (1987). 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 80, 1784-1793.
14. Chan CP, Hansen RJ & Stern JS (1985). Protein turnover in insulin-treated, alloxan-diabetic lean and obese Zucker rats. J Nutr 115, 959-969.
15. Chanseaume E, Giraudet C, Gryson C, Walrand S, Rousset P, Boirie Y & Morio B (2007). Enhanced muscle mixed and mitochondrial protein synthesis rates after a high-fat or high-sucrose diet. Obesity (Silver Spring) 15, 853-859.
16. Cuthbertson D, Smith K, Babraj J, Leese G, Waddell T, Atherton P, Wackerhage H, Taylor PM & Rennie MJ (2005). Anabolic signaling deficits underlie amino acid resistance of wasting, aging muscle. FASEB J 19, 422-424.
17. de Ferranti S & Mozaffarian D (2008). The perfect storm: obesity, adipocyte dysfunction, and metabolic consequences. Clin Chem 54, 945-955.
18. Dunn MA & Hartsook EW (1980). Comparative amino acid and protein metabolism in obese and non-obese Zucker rats. J Nutr 110, 1865-1879.
19. Durschlag RP & Layman DK (1983). Skeletal muscle growth in lean and obese Zucker rats. Growth 47, 282-291.
20. Estornell E, Cabo J & Barber T (1995). Protein synthesis is stimulated in nutritionally obese rats. J Nutr 125, 1309-1315.
21. Fluckey JD, Cortright RN, Tapscott E, Koves T, Smith L, Pohnert S & Dohm GL (2004). Active involvement of PKC for insulin-mediated rates of muscle protein synthesis in Zucker rats. Am J Physiol Endocrinol Metab 286, E753-E758.
22. Fluckey JD, Pohnert SC, Boyd SG, Cortright RN, Trappe TA & Dohm GL (2000). Insulin stimulation of muscle protein synthesis in obese Zucker rats is not via a rapamycin-sensitive pathway. Am J Physiol Endocrinol Metab 279, E182-187.
23. Forbes GB & Welle SL (1983). Lean body mass in obesity. Int J Obes (Lond) 7, 99-107.
24. Friedman JE, Lemon PW & Finkelstein JA (1990). Effect of exercise and obesity on skeletal muscle amino acid uptake. J Appl Physiol 69, 1347-1352.
25. Goodpaster BH, Theriault R, Watkins SC & Kelley DE (2000). Intramuscular lipid content is increased in obesity and decreased by weight loss. Metabolism 49, 467-472.
26. Guillet C, Delcourt I, Rance M, Giraudet C, Walrand S, Bedu M, Duche P & Boirie Y (2009). Changes in basal and insulin and amino acid response of whole body and skeletal muscle proteins in obese men. J Clin Endocrinol Metab 94, 3044-3050.
27. Guillet C, Masgrau A & Boirie Y (2011). Is protein metabolism changed with obesity? Curr Opin Clin Nutr Metab Care 14, 89-92.
28. Guillet C, Prod'homme M, Balage M, Gachon P, Giraudet C, Morin L, Grizard J & Boirie Y (2004a). Impaired anabolic response of muscle protein synthesis is associated with S6K1 dysregulation in elderly humans. FASEB J 18, 1586-1587.
29. Guillet C, Zangarelli A, Gachon P, Morio B, Giraudet C, Rousset P & Boirie Y (2004b). Whole body protein breakdown is less inhibited by insulin, but still responsive to amino acid, in nondiabetic elderly subjects. J Clin Endocrinol Metab 89, 6017-6024.
30. Guillet C, Zangarelli A, Mishellany A, Rousset P, Sornet C, Dardevet D & Boirie Y (2004c). Mitochondrial and sarcoplasmic proteins, but not myosin heavy chain, are sensitive to leucine supplementation in old rat skeletal muscle. Exp Gerontol 39, 745-751.
31. Hamrick MW, Pennington C, Newton D, Xie D & Isales C (2004). Leptin deficiency produces contrasting phenotypes in bones of the limb and spine. Bone 34, 376-383.
32. Haslam DW & James WP (2005). Obesity. Lancet 366, 1197-1209.
33. Hay N & Sonenberg N (2004). Upstream and downstream of mTOR. Genes Dev 18, 1926-1945.
34. Heymsfield SB, Smith R, Aulet M, Bensen B, Lichtman S, Wang J & Pierson RN Jr (1990). Appendicular skeletal muscle mass: measurement by dual-photon absorptiometry. Am J Clin Nutr 52, 214-218.
35. Hulens M, Vansant G, Lysens R, Claessens AL, Muls E & Brumagne S (2001). Study of differences in peripheral muscle strength of lean versus obese women: an allometric approach. Int J Obes Relat Metab Disord 25, 676-681.
36. Janssen I, Heymsfield SB, Wang ZM & Ross R (2000). Skeletal muscle mass and distribution in 468 men and women aged 18-88 yr. J Appl Physiol 89, 81-88.
37. Kaneko S, Iida RH, Suga T, Fukui T, Morito M & Yamane A (2011). Changes in triacylglycerol-accumulated fiber type, fiber type composition, and biogenesis in the mitochondria of the soleus muscle in obese rats. Anat Rec (Hoboken) 294, 1904-1912.
38. Katsanos CS & Mandarino LJ (2011). Protein metabolism in human obesity: a shift in focus from whole-body to skeletal muscle. Obesity (Silver Spring) 19, 469-475.
39. Kemp JG, Blazev R, Stephenson DG & Stephenson GM (2009). Morphological and biochemical alterations of skeletal muscles from the genetically obese (ob/ob) mouse. Int J Obes (Lond) 33, 831-841.
40. Kim J, Wang Z, Heymsfield SB, Baumgartner RN & Gallagher D (2002). Total-body skeletal muscle mass: estimation by a new dual-energy X-ray absorptiometry method. Am J Clin Nutr 76, 378-383.
41. Krssak M, Falk Petersen K, Dresner A, DiPietro L, Vogel SM, Rothman DL, Roden M & Shulman GI (1999). Intramyocellular lipid concentrations are correlated with insulin sensitivity in humans: a 1H NMR spectroscopy study. Diabetologia 42, 113-116.
42. Lang CH (2006). Elevated plasma free fatty acids decrease basal protein synthesis, but not the anabolic effect of leucine, in skeletal muscle. Am J Physiol Endocrinol Metab 291, E666-E674.
43. Lillioja S, Young AA, Culter CL, Ivy JL, Abbott WG, Zawadzki JK, Yki-Jarvinen H, Christin L, Secomb TW & Bogardus C (1987). Skeletal muscle capillary density and fiber type are possible determinants of in vivo insulin resistance in man. J Clin Invest 80, 415-424.
44. Louard RJ, Fryburg DA, Gelfand RA & Barrett EJ (1992). Insulin sensitivity of protein and glucose metabolism in human forearm skeletal muscle. J Clin Invest 90, 2348-2354.
45. Maffiuletti NA, Jubeau M, Munzinger U, Bizzini M, Agosti F, De Col A, Lafortuna CL & Sartorio A (2007). Differences in quadriceps muscle strength and fatigue between lean and obese subjects. Eur J Appl Physiol 101, 51-59.
46. Moro C, Galgani JE, Luu L, Pasarica M, Mairal A, Bajpeyi S, Schmitz G, Langin D, Liebisch G & Smith SR (2009). Influence of gender, obesity, and muscle lipase activity on intramyocellular lipids in sedentary individuals. J Clin Endocrinol Metab 94, 3440-3447.
47. Nilsson MI, Greene NP, Dobson JP, Wiggs MP, Gasier HG, Macias BR, Shimkus KL & Fluckey JD (2010). Insulin resistance syndrome blunts the mitochondrial anabolic response following resistance exercise. Am J Physiol Endocrinol Metab 299, E466-E474.
48. Oosterveer MH, van Dijk TH, Tietge UJ, Boer T, Havinga R, Stellaard F, Groen AK, Kuipers F & Reijngoud DJ (2009). High fat feeding induces hepatic fatty acid elongation in mice. PloS One 4, e6066.
49. Patterson BW, Horowitz JF, Wu G, Watford M, Coppack SW & Klein S (2002). Regional muscle and adipose tissue amino acid metabolism in lean and obese women. Am J Physiol Endocrinol Metab 282, E931-E936.
50. Perseghin G, Scifo P, De Cobelli F, Pagliato E, Battezzati A, Arcelloni C, Vanzulli A, Testolin G, Pozza G, Del Maschio A & Luzi L (1999). 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 48, 1600-1606.
51. Pietilainen KH, Sysi-Aho M, Rissanen A, Seppanen-Laakso T, Yki-Jarvinen H, Kaprio J & Oresic M (2007). Acquired obesity is associated with changes in the serum lipidomic profile independent of genetic effects - a monozygotic twin study. PloS One 2, e218.
52. Reeds PJ, Haggarty P, Wahle KW & Fletcher JM (1982). Tissue and whole-body protein synthesis in immature Zucker rats and their relationship to protein deposition. Biochem J 204, 393-398.
53. Rennie MJ (2009). Anabolic resistance in critically ill patients. Crit Care Med 37, S398-S399.
54. Samuel VT, Petersen KF & Shulman GI (2010). Lipid-induced insulin resistance: unravelling the mechanism. Lancet 375, 2267-2277.
55. 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.
56. Sessions VA & Salter AM (1994). The effects of different dietary fats and cholesterol on serum lipoprotein concentrations in hamsters. Biochim Biophys Acta 1211, 207-214.
57. Shargill NS, Ohshima K, Bray GA & Chan TM (1984). Muscle protein turnover in the perfused hindquarters of lean and genetically obese-diabetic (db/db) mice. Diabetes 33, 1160-1164.
58. Simoneau JA, Colberg SR, Thaete FL & Kelley DE (1995). Skeletal muscle glycolytic and oxidative enzyme capacities are determinants of insulin sensitivity and muscle composition in obese women. FASEB J 9, 273-278.
59. Sinitskaya N, Gourmelen S, Schuster-Klein C, Guardiola-Lemaitre B, Pevet P & Challet E (2007). Increasing the fat-to-carbohydrate ratio in a high-fat diet prevents the development of obesity but not a prediabetic state in rats. Clin Sci (Lond) 113, 417-425.
60. Slawik M & Vidal-Puig AJ (2007). Adipose tissue expandability and the metabolic syndrome. Genes Nutr 2, 41-45.
61. Sridhar MG, Vinayagamoorthi R, Arul Suyambunathan V, Bobby Z & Selvaraj N (2008). Bitter gourd (Momordica charantia) improves insulin sensitivity by increasing skeletal muscle insulin-stimulated IRS-1 tyrosine phosphorylation in high-fat-fed rats. Br J Nutr 99, 806-812.
62. Tanner CJ, Barakat HA, Dohm GL, Pories WJ, MacDonald KG, Cunningham PR, Swanson MS & Houmard JA (2002). Muscle fiber type is associated with obesity and weight loss. Am J Physiol Endocrinol Metab 282, E1191-E1196.
63. Vinayagamoorthi R, Bobby Z & Sridhar MG (2008). Antioxidants preserve redox balance and inhibit c-Jun-N-terminal kinase pathway while improving insulin signaling in fat-fed rats: evidence for the role of oxidative stress on IRS-1 serine phosphorylation and insulin resistance. J Endocrinol 197, 287-296.
64. Virkamaki A, Korsheninnikova E, Seppala-Lindroos A, Vehkavaara S, Goto T, Halavaara J, Hakkinen AM & Yki-Jarvinen H (2001). 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 50, 2337-2343.
65. Virtue S & Vidal-Puig A (2010). Adipose tissue expandability, lipotoxicity and the Metabolic Syndrome - an allostatic perspective. Biochim Biophys Acta 1801, 338-349.
66. Volpi E, Mittendorfer B, Rasmussen BB & Wolfe RR (2000). The response of muscle protein anabolism to combined hyperaminoacidemia and glucose-induced hyperinsulinemia is impaired in the elderly. J Clin Endocrinol Metab 85, 4481-4490.
67. Weinstein RB, Tritschler HJ & Henriksen EJ (2001). Antioxidant alpha-lipoic acid and protein turnover in insulin-resistant rat muscle. Free RadicBiol Med 30, 383-388.
68. Zaman MQ, Leray V, Le Bloc'h J, Thorin C, Ouguerram K & Nguyen P (2011). Lipid profile and insulin sensitivity in rats fed with high-fat or high-fructose diets. Br J Nutr 106, S206-S210.
69. Zamboni M, Mazzali G, Fantin F, Rossi A & Di Francesco V (2008). Sarcopenic obesity: a new category of obesity in the elderly. Nutr Metab Cardiovasc Dis 18, 388-395.
70. Zangarelli A, Chanseaume E, Morio B, Brugere C, Mosoni L, Rousset P, Giraudet C, Patrac V, Gachon P, Boirie Y & Walrand S (2006). Synergistic effects of caloric restriction with maintained protein intake on skeletal muscle performance in 21-month-old rats: a mitochondria-mediated pathway. FASEB J 20, 2439-2450.
71. Zangarelli A, Walrand S, Guillet C, Gachon P, Rousset P, Giraudet C, Picard B & Boirie Y (2004). Centrifugation- based isolation of myosin for measurement of its synthesis rate in small muscle samples. Anal Biochem 327, 55-60.