Leptin and leucine synergistically regulate protein metabolism in C2C12 myotubes and mouse skeletal muscles

British Journal of Nutrition

Volumn 110, Issue 2, 2013, Pages 256-264

  Mao, Xiangbing ^a   Zeng, Xiangfang ^a   Huang, Zhimin ^a   Wang, Junjun ^a   Qiao, Shiyan ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

C2C12 myotubes; Leptin; Leucine; Mouse skeletal muscles; Protein metabolism

Indexed keywords

AMINO ACID; BETA ACTIN; LEPTIN; LEPTIN RECEPTOR; LEUCINE; UREA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DIET SUPPLEMENTATION; DIETARY INTAKE; DRUG POTENTIATION; ENZYME DEGRADATION; ENZYME INHIBITION; ENZYME REGULATION; GASTROCNEMIUS MUSCLE; IN VITRO STUDY; MALE; MOUSE; MUSCLE FIBRIL; NONHUMAN; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEIN SYNTHESIS; SKELETAL MUSCLE; SOLEUS MUSCLE; UREA BLOOD LEVEL;

ANIMALS; CELL LINE; DIETARY SUPPLEMENTS; DRUG SYNERGISM; LEPTIN; LEUCINE; MICE; MICE, KNOCKOUT; MICE, OBESE; MUSCLE FIBERS, SKELETAL; MUSCLE PROTEINS; MUSCLE, SKELETAL; OBESITY; ORGAN SIZE; PROTEIN BIOSYNTHESIS; PROTEOLYSIS; RECEPTORS, LEPTIN; RECOMBINANT PROTEINS; UREA;

MUS;

EID: 84879178563     PISSN: 00071145     EISSN: 14752662     Source Type: Journal    
DOI: 10.1017/S0007114512004849     Document Type: Article

References (56)

1. Anthony JC, Reiter AK, Anthony TG, et al. (2002) Orally administered leucine enhances protein synthesis in skeletal muscle of diabetic rats in the absence of increases in 4E-BP1 or S6K1 phosphorylation. Diabetes 51, 928-936.
2. Newgard CB, An J, Bain JR, et al. (2009) A branched-chain amino acid-related metabolic signature that differentiates obese and lean humans and contributes to insulin resistance. Cell Metab 9, 311-326.
3. Du M, Shen QW, Zhu MJ, et al. (2007) Leucine stimulates mammalian target of rapamycin signaling in C2C12 myoblasts in part through inhibition of adenosine monophosphate-activated protein kinase. J Anim Sci 85, 919-927.
4. O'Connor PMJ, Bush JA, Suryawan A, et al. (2003) Insulin and amino acids independently stimulate skeletal muscle protein synthesis in neonatal pigs. Am J Physiol 284, E110-E119.
5. Norton LE, Layman DK, Bunpo P, et al. (2009) The leucine content of a complete meal directs peak activation but not duration of skeletal muscle protein synthesis and mammalian target of rapamycin signaling in rats. J Nutr 139, 1103-1109.
6. Combaret L, Dardevet D, Rieu I, et al. (2005) A leucinesupplemented diet restores the defective postprandial inhibition of proteasome-dependent proteolysis in aged rat skeletal muscle. J Physiol 569, 489-499.
7. Mitchell JC, Evenson AR & Tawa NE (2004) Leucine inhibits proteolysis by the mTOR kinase signaling pathway in skeletal muscle. J Surg Res 121, 311.
8. Nakashima K, Ishida A, Yamazaki M, et al. (2005) Leucine suppresses myofibrillar proteolysis by down-regulating ubiquitin-proteasome pathway in chick skeletal muscles. Biochem Biophys Res Commun 336, 660-666.
9. Yin YL, Yao K, Liu ZJ, et al. (2010) Supplementing L-leucine to a low-protein diet increases tissue protein synthesis in weanling pigs. Amino Acids 39, 1477-1486.
10. Li FN, Yin YL, Tan BE, et al. (2011) Leucine nutrition in animals and humans: mTOR signaling 3 and beyond. Amino Acids 41, 1185-1193.
11. Lynch CJ, Hutson SM, Patson BJ, et al. (2002) Tissue-specific effects of chronic dietary leucine and norleucine supplementation on protein synthesis in rats. Am J Physiol 283, E824-E835.
12. Roh C, Han JR, Tzatsos A, et al. (2003) Nutrient-sensing mTOR-mediated pathway regulates leptin production in isolated rat adipocytes. Am J Physiol 284, E322-E330.
13. Zhang YY, Proenca R, Maffei M, et al. (1994) Positional cloning of the mouse obese gene and its human homologue. Nature 372, 425-432.
14. Maffei M, Halaas J, Ravussin E, et al. (1995) Leptin levels in human and rodent: measurement of plasma leptin and ob RNA in obese and weight reduced subjects. Nat Med 1, 1155-1161.
15. Tartaglia LA (1997) The leptin receptor. J Biol Chem 272, 6093-6096.
16. Schwartz MW, Baskin DG, Kaiyala KJ, et al. (1999) Model for the regulation of energy balance and adiposity by the central nervous system. Am J Clin Nutr 69, 584-596.
17. Carbo N, Ribas V, Busquets S, et al. (2000) Short-term effects of leptin on skeletal muscle protein metabolism in the rat. J Nutr Biochem 11, 431-435.
18. Ramsay TG (2003) Procine leptin inhibits protein breakdown and stimulates fatty acid oxidation in C2C12 myotubes. J Anim Sci 81, 3046-3051.
19. Lamosova D & Zeman M (2001) Effect of leptin and insulin on chick embryonic muscle cells and hepatocytes. Physiol Res 50, 183-189.
20. Tartaglia LA, Dembski M, Weng X, et al. (1995) Identification and expression cloning of a leptin receptor, OB-R. Cell 83, 1263-1271.
21. Chua SC, Chung WK, Wu-Peng XS, et al. (1996) Phenotypes of mouse diabetes and rat fatty due to mutations in the OB (leptin) receptor. Science 271, 994-996.
22. Chen XJ, Li DF, Yin JD, et al. (2006) Regulation of dietary energy level and oil source on leptin and its long form receptor mRNA expression of the adipose tissues in growing pigs. Domest Anim Endocrinol 31, 269-283.
23. Koros C, Boukouvalas G, Gerozissis K, et al. (2009) Fat diet affects leptin receptor levels in the rat cerebellum. Nutrition 25, 85-87.
24. Alonso A, Fernandez R, Moreno M, et al. (2007) Leptin and its receptor are controlled by 17b-estradiol in peripheral tissue of ovariectomized rats. Exp Biol Med 232, 542-549.
25. Mao XB, Zeng XF, Wang JJ, et al. (2011) Leucine promotes leptin receptor expression in mouse C2C12 myotubes through the mTOR pathway. Mol Biol Rep 38, 3201-3206.
26. Miyanaga F, Ogawa Y, Ebihara K, et al. (2003) Leptin as an adjunct of insulin therapy in insulin-deficient diabetes. Diabetologia 46, 1329-1337.
27. Carvalheira JBC, Siloto RMP, Ignacchitti I, et al. (2001) Insulin modulates leptin-induced STAT3 activation in rat hypothalamus. FEBS Lett 500, 119-124.
28. Han B, Tong J, Zhu MJ, et al. (2008) Insulin-like growth factor-1 (IGF-1) and leucine activate pig myogenic satellite cells through mammalian target of rapamycin (mTOR) pathway. Mol Reprod Dev 75, 810-817.
29. Fang X, Fetros J, Dadson KE, et al. (2009) Leptin prevents the metabolic effects of adiponectin in L6 myotubes. Diabetologia 52, 2190-2200.
30. Sadagurski M, Norquay L, Farhang J, et al. (2010) Human IL6 enhances leptin action in mice. Diabetologia 53, 525-535.
31. Berti L & Gammeltoft S (1999) Leptin stimulates glucose uptake in mouse C2C12 muscle cells by activation of ERK2. Mol Cell Endocrinol 157, 121-130.
32. Wang X, Qiao SY, Yin YL, et al. (2007) A deficiency or excess of dietary threonine reduces protein synthesis in jejunum and skeletal muscle of young pigs. J Nutr 137, 1442-1446.
33. Le Bacquer O, Nazih H, Blottiere H, et al. (2001) Effects of glutamine deprivation on protein synthesis in a model of human enterocytes in culture. Am J Physiol 281, G1340-G1347.
34. Kanazawa T, Taneike I, Akaishi R, et al. (2004) Amino acids and insulin control autophagic proteolysis through different signaling pathways in relation to mTOR in isolated rat hepatocytes. J Biol Chem 279, 8452-8459.
35. Zeng XF, Wang FL, Fan X, et al. (2008) Dietary arginine supplementation during early pregnancy enhances embryonic survival in rats. J Nutr 138, 1421-1425.
36. Lowry OH, Rosebrough NJ, Farr AL, et al. (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193, 265-275.
37. Matsuzaki K, Kato H, Sakai R, et al. (2005) Transcriptomics and metabolomics of dietary leucine excess. J Nutr 135, 1571S-1575S.
38. Edmonds MS & Baker DH (1987) Amino acid excesses for young pigs: effects of excess methionine, tryptophan, threonine or leucine. J Anim Sci 64, 1664-1671.
39. Mao XB, Zeng XF, Cai CJ, et al. (2011) Effect of dietary leucine supplementation on plasma leptin level and protein metabolism of skeletal muscles in rats. Chinese J Anim Sci 47, 26-30.
40. Picard F, Richard D, Huang Q, et al. (1998) Effects of leptin adipose tissue lipoprotein lipase in the obese ob/ob mouse. Int J Obes Relat Metab Disord 22, 1088-1095.
41. Pelleymounter MA, Cullen MJ, Baker MB, et al. (1995) Effects of the obese gene product on body weight regulation in ob/ob mice. Science 269, 540-543.
42. Schaefer AL & Scott SL (1993) Amino acid flooding doses for measuring rates of protein synthesis. Amino Acids 4, 5-19.
43. Bregendahl K, Liu LJ, Cant JP, et al. (2004) Fractional protein synthesis rates measured by an intraperitoneal injection of a flooding dose of L-[ring-2H5] phenylalanine in pigs. J Nutr 134, 2722-2728.
44. Tawa NE & Goldberg AL (1992) Suppression of muscle protein turnover and amino acid degradation by dietary protein deficiency. Am J Physiol 263, E317-E325.
45. Suryawan A, Nguyen HV, Bush JA, et al. (2001) Developmental changes in the feeding-induced activation of the insulin-signaling pathway in neonatal pigs. Am J Physiol 281, E908-E915.
46. Zhang Y, Guo K, LeBlanc RE, et al. (2007) Increasing dietary leucine intake reduces diet-induced obesity and improves glucose and cholesterol metabolism in mice via multimechanisms. Diabetes 56, 1647-1654.
47. Rieu I, Sornet C, Bayle G, et al. (2003) Leucinesupplemented meal feeding for ten days beneficially affects postprandial muscle protein synthesis in old rats. J Nutr 133, 1198-1205.
48. Coma J, Carrion D & Zimmerman DR (1995) Use of plasma urea nitrogen as a rapid response criterion to determine the lysine requirement of pigs. J Anim Sci 73, 472-481.
49. Suryawan A, Jeyapalan AS, Orellana RA, et al. (2008) Leucine stimulates protein synthesis in skeletal muscle of neonatal pigs by enhancing mTORC1 activation. Am J Physiol 295, E868-E875.
50. Sugawara T, Ito Y, Nishizawa N, et al. (2009) Regulation of muscle protein degradation, not synthesis, by dietary leucine in rats fed a protein-deficient diet. Amino Acids 37, 609-616.
51. Escobar J, Frank JW, Suryawan A, et al. (2006) Regulation of cardiac and skeletal muscle protein synthesis by individual branched-chain amino acids in neonatal pigs. Am J Physiol 290, E612-E621.
52. Lynch CJ, Gern B, Lloyd C, et al. (2006) Leucine in food mediates some of the postprandial rise in plasma leptin concentrations. Am J Physiol 291, E621-E630.
53. Tomiya T, Nishikawa T, Inoue Y, et al. (2007) Leucine stimulates HGF production by hepatic stellate cells through mTOR pathway. Biochem Biophys Res Commun 358, 176-180.
54. Ijichi C, Matsumura T, Tsuji T, et al. (2003) Branched-chain amino acids promote albumin synthesis in rat primary hepatocytes through the mTOR signal transduction system. Biochem Biophys Res Commun 303, 59-64.
55. Li FN, Yang HS, Duan YH, et al. (2011) Myostatin regulates preadipocyte differentiation and lipid metabolism of adipocyte via ERK1/2. Cell Biol Int 35, 1141-1146.
56. Yang HS, Li FN, Kong XF, et al. (2012) Molecular cloning, tissue distribution and ontogenetic expression of Xiang pig Chemerin and its involvement in regulating energy metabolism through Akt and ERK1/2 signaling pathways. Mol Biol Rep 39, 1887-1894.