Circulating branched-chain amino acid concentrations are associated with obesity and future insulin resistance in children and adolescents

Pediatric Obesity

Volumn 8, Issue 1, 2013, Pages 52-61

  Mccormack, S E ^a,b   Shaham, O ^c,d   Mccarthy, M A ^a   Deik, A A ^c   Wang, T J ^a,e   Gerszten, R E ^a,c   Clish, C B ^c   Mootha, V K ^a,c   Grinspoon, S K ^a   Fleischman, A ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^d IBM RESEARCH   (United States)

^e BOSTON UNIVERSITY   (United States)

Author keywords

Branched chain amino acids; Insulin resistance; Metabolomics; Paediatric obesity

Indexed keywords

BRANCHED CHAIN AMINO ACID; ISOLEUCINE; LEUCINE; VALINE;

ADOLESCENT; ADULT; ARTICLE; BODY MASS; CHILD; CHILDHOOD OBESITY; FEMALE; HUMAN; INSULIN RESISTANCE; MALE; PRIORITY JOURNAL; SCHOOL CHILD;

EID: 84874800752     PISSN: 20476302     EISSN: 20476310     Source Type: Journal    
DOI: 10.1111/j.2047-6310.2012.00087.x     Document Type: Article

References (45)

1. Danaei G, Finucane MM, Lu Y, et al. National, regional, and global trends in fasting plasma glucose and diabetes prevalence since 1980: Systematic analysis of health examination surveys and epidemiological studies with 370 country-years and 2.7 million participants. Lancet 2011; 378: 31-40.
2. Ten S, Maclaren N. Insulin resistance syndrome in children. J Clin Endocrinol Metab 2004; 89: 2526-2539.
3. Amiel SA, Sherwin RS, Simonson DC, Lauritano AA, Tamborlane WV. Impaired insulin action in puberty: A contributing factor to poor glycemic control in adolescents with diabetes. N Engl J Med 1986; 315: 215-219.
4. Pinhas-Hamiel O, Zeitler P. The global spread of type 2 diabetes mellitus in children and adolescents. J Pediatr 2005; 146: 693-700.
5. Felig P, Marliss E, Cahill GF, Jr. Plasma amino acid levels and insulin secretion in obesity. N Engl J Med 1969; 281: 811-816.
6. Matthews DE. Observations of branched-chain amino acid administration in humans. J Nutr 2005; 135 (Suppl. 6): 1580S-1584S.
7. Buse MG, Biggers JF, Friderici KH, Buse JF. Oxidation of branched-chain amino acids by isolated hearts and diaphragms of the rat. The effect of fatty acids, glucose, and pyruvate respiration. J Biol Chem 1972; 247: 8085-8096.
8. Patti ME, Brambilla E, Luzi L, Landaker EJ, Kahn CR. Bidirectional modulation of insulin action by amino acids. J Clin Invest 1998; 101: 1519-1529.
9. Krebs M, Krssak M, Bernroider E, et al. Mechanism of amino acid-induced skeletal muscle insulin resistance in humans. Diabetes 2002; 51: 599-605.
10. Newgard CB, An J, Bain JR, et al. A branched-chain amino acid-related metabolic signature that differentiates obese and lean humans and contributes to insulin resistance. Cell Metab 2009; 9: 311-326.
11. Wang TJ, Larson MG, Vasan RS, et al. Metabolite profiles and the risk of developing diabetes. Nat Med 2011; 17: 448-453.
12. Chaussain JL, Georges P, Olive G, Job JC. Effect of 24 hour fast in obese children. Biomedicine 1976; 25: 299-302.
13. Molnar D, Soltesz G. Metabolic and hormonal effects of fasting in obese children. Acta Paediatr Acad Sci Hung 1982; 23: 45-50.
14. Fleischman A, Kron M, Systrom DM, Hrovat M, Grinspoon SK. Mitochondrial function and insulin resistance in overweight and normal-weight children. J Clin Endocrinol Metab 2009; 94: 4923-4930.
15. Fleischman A, Makimura H, Stanley TL, et al. Skeletal muscle phosphocreatine recovery after submaximal exercise in children and young and middle-aged adults. J Clin Endocrinol Metab 2010; 95: E69-E74.
16. McCormack SE, McCarthy MA, Farilla L, et al. Skeletal muscle mitochondrial function is associated with longitudinal growth velocity in children and adolescents. J Clin Endocrinol Metab 2011; 96: E1612-E1618.
17. 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.
18. Gungor N, Saad R, Janosky J, Arslanian S. Validation of surrogate estimates of insulin sensitivity and insulin secretion in children and adolescents. J Pediatr 2004; 144: 47-55.
19. Matsuda M, DeFronzo RA. Insulin sensitivity indices obtained from oral glucose tolerance testing: Comparison with the euglycemic insulin clamp. Diabetes Care 1999; 22: 1462-1470.
20. Kriska AM, Knowler WC, LaPorte RE, et al. Development of questionnaire to examine relationship of physical activity and diabetes in Pima Indians. Diabetes Care 1990; 13: 401-411.
21. Bland JM, Altman DG. Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1986; 1: 307-310.
22. Shaham O, Slate NG, Goldberger O, et al. A plasma signature of human mitochondrial disease revealed through metabolic profiling of spent media from cultured muscle cells. Proc Natl Acad Sci U S A 2010; 107: 1571-1575.
23. Pozefsky T, Felig P, Tobin JD, Soeldner JS, Cahill GF, Jr. Amino acid balance across tissues of the forearm in postabsorptive man. Effects of insulin at two dose levels. J Clin Invest 1969; 48: 2273-2282.
24. Shaham O, Wei R, Wang TJ, et al. Metabolic profiling of the human response to a glucose challenge reveals distinct axes of insulin sensitivity. Mol Syst Biol 2008; 4: Article Number 214: 1-8.
25. 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.
26. Shah SH, Crosslin DR, Haynes CS, et al. Branchedchain amino acid levels are associated with improvement in insulin resistance with weight loss. Diabetologia 2012; 55: 321-330.
27. Laferrere B, Reilly D, Arias S, et al. Differential metabolic impact of gastric bypass surgery versus dietary intervention in obese diabetic subjects despite identical weight loss. Sci Transl Med 2011; 3: 80re2.
28. Rocha DM, Faloona GR, Unger RH. Glucagonstimulating activity of 20 amino acids in dogs. J Clin Invest 1972; 51: 2346-2351.
29. Nair KS, Short KR. Hormonal and signaling role of branched-chain amino acids. J Nutr 2005; 135 (Suppl. 6): 1547S-1552S.
30. Di Cairano ES, Davalli AM, Perego L, et al. The glial glutamate transporter 1 (GLT1) is expressed by pancreatic {beta}-cells and prevents glutamate-induced {beta}-cell death. J Biol Chem 2011; 286: 14007-14018.
31. Macotela Y, Emanuelli B, Bang AM, et al. Dietary leucine-an environmental modifier of insulin resistance acting on multiple levels of metabolism. PLoS ONE 2011; 6: E21187.
32. Newgard CB. Interplay between lipids and branchedchain amino acids in development of insulin resistance. Cell Metab 2012; 15: 606-614.
33. Gruber HJ, Mayer C, Mangge H, Fauler G, Grandits N, Wilders-Truschnig M. Obesity reduces the bioavailability of nitric oxide in juveniles. Int J Obes (Lond) 2008; 32: 826-831.
34. Thomas SR, Witting PK, Stocker R. 3-Hydroxyanthranilic acid is an efficient, cell-derived co-antioxidant for alpha-tocopherol, inhibiting human low density lipoprotein and plasma lipid peroxidation. J Biol Chem 1996; 271: 32714-32721.
35. Baran H, Staniek K, Kepplinger B, Stur J, Draxler M, Nohl H. Kynurenines and the respiratory parameters on rat heart mitochondria. Life Sci 2003; 72: 1103-1115.
36. Fernstrom JD. Branched-chain amino acids and brain function. J Nutr 2005; 135 (Suppl. 6): 1539S-1546S.
37. Arslanian SA, Kalhan SC. Protein turnover during puberty in normal children. Am J Physiol 1996; 270 (1 Pt 1): E79-E84.
38. Amiel SA, Caprio S, Sherwin RS, Plewe G, Haymond MW, Tamborlane WV. Insulin resistance of puberty: A defect restricted to peripheral glucose metabolism. J Clin Endocrinol Metab 1991; 72: 277-282.
39. Balagopal P, Bayne E, Sager B, Russell L, Patton N, George D. Effect of lifestyle changes on whole-body protein turnover in obese adolescents. Int J Obes Relat Metab Disord 2003; 27: 1250-1257.
40. 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.
41. 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.
42. Kanaley JA, Haymond MW, Jensen MD. Effects of exercise and weight loss on leucine turnover in different types of obesity. Am J Physiol 1993; 264 (5 Pt 1): E687-E692.
43. Caballero B, Wurtman RJ. Differential effects of insulin resistance on leucine and glucose kinetics in obesity. Metabolism 1991; 40: 51-58.
44. Motil KJ, Bier DM, Matthews DE, Burke JF, Young VR. Whole body leucine and lysine metabolism studied with [1-13C]leucine and [alpha-15N]lysine: Response in healthy young men given excess energy intake. Metabolism 1981; 30: 783-791.
45. Goulet O, DePotter S, Salas J, et al. Leucine metabolism at graded amino acid intakes in children receiving parenteral nutrition. Am J Physiol 1993; 265 (4 Pt 1): E540-E546.