Academia.eduAcademia.edu

Outline

The Role of Leucine in Weight Loss Diets and Glucose Homeostasis

2003, Journal of Nutrition

https://doi.org/10.1093/JN/133.1.261S

Abstract

Debate about the optimum balance of macronutrients for adult weight maintenance or weight loss continues to expand. Often this debate centers on the relative merits or risks of carbohydrates vs. fats; however, there is increasing interest in the optimal level of dietary protein for weight loss. Diets with a reduced ratio of carbohydrates/protein are reported to be beneficial for weight loss, although diet studies appear to lack a fundamental hypothesis to support higher protein intakes. Presently, needs for dietary proteins are established by the recommended daily allowance (RDA) as the minimum level of protein necessary to maintain nitrogen balance. The RDA define the primary use of amino acids as substrates for synthesis of body proteins. There is emerging evidence that additional metabolic roles for some amino acids require plasma and intracellular levels above minimum needs for protein synthesis. The branched-chain amino acid leucine is an example of an amino acid with numerous metabolic roles that function in proportion with cellular concentration. This review provides an overview of the current understanding of metabolic roles of leucine and proposes a metabolic framework to evaluate the merits of a higher protein diet for weight loss.

References (64)

  1. Must, A., Spadano, J., Coakley, E. H., Field, A. E., Colditz, G. & Dietz, W. H. (1999) The disease burden associated with overweight and obesity. J. Am. Med. Assoc. 282: 1523-1529.
  2. Surgeon General's Report on Nutrition and Health. (1988) USDHHS Publication no. 88-50210, Public Health Service, Washington, D.C.
  3. American Heart Association: Scientific Statement. (2000) AHA Dietary Guidelines Revison 2000: a statement for healthcare professionals from the Nutrition Committee of the American Heart Association. Circulation 102: 2284 - 2299.
  4. FASEB, Life Sciences Research Office. (1995) Third Report on Nutri- tion Monitoring in the United States. U.S. Government Printing Office, Washing- ton, D.C.
  5. Cahill, G. F. (1970) Starvation in man. N. Engl. J. Med. 282: 668 -675.
  6. Flatt, J. P. (1995) Use and storage of carbohydrate and fat. Am. J. Clin. Nutr. 61(suppl.): 925S.
  7. McGarry, J. D. (1998) Glucose-fatty acid interactions in health and disease. Am. J. Clin. Nutr. 67(suppl.): 500S-504S.
  8. Wolfe, R. R. (1998) Metabolic interactions between glucose and fatty acids in humans. Am. J. Clin. Nutr. 67(suppl.): 519S-526S.
  9. Wolfe, B. M. & Giovannetti, P. M. (1991) Short-term effects of substi- tuting protein for carbohydrate in diets of moderately hypercholesterolemic hu- man subjects. Metabolism 40: 338 -343.
  10. Parker, B., Noakes, M., Luscombe, N. & Clifton, P. (2002) Effect of a high-protein, monounsaturated fat weight loss diet on glycemic control and lipid levels in type 2 diabetes. Diabetes Care 25: 425-430.
  11. Sidossis, L. S., Mittendorfer, B., Walser, E., Chinkes, D. & Wolfe, R. R.
  12. Hyperglycemia-induced inhibition of splanchnic fatty acid oxidation in- creases hepatic triacylglycerol secretion. Am. J. Physiol. Endocrinol. Metab. 275: E798 -E805.
  13. Ludwig, D. S., Majzoub, J. A., Al-Zahrani, A., Dallal, G. E., Blanco, I. & Roberts. S. B. (1999) High glycemic index foods, overeating, and obesity. Pediatrics 103: E261-E266.
  14. Food and Nutrition Board, National Academy of Science. (1994) How Should the Recommended Dietary Allowances Be Revised? National Academy Press, Washington, D.C.
  15. Waterlow, J. C., Garlick, P. J. & Millward, D. J. (1978) Protein Turnover in Mammalian Tissues and in the Whole Body. Elsevier-North Holland, Amster- dam, The Netherlands.
  16. Wolfe, R. R., Wolfe, M. H., Nadel, E. R. & Shaw, J.H.F. (1984) Isotopic determination of amino acid-urea interactions in exercise in humans. J. Appl. Physiol. 56: 221-229.
  17. Hutson, S. M. & Harris, R. A. (2001) Leucine as a nutritional signal. J. Nutr. 131: 839S-840S.
  18. Layman, D. K. (2002) Role of leucine in protein metabolism during exercise and recovery. Can. J. Appl. Physiol. 27(6): 592-608.
  19. Harper, A. E., Miller, R. H. & Block, K. P. (1984) Branched-chain amino acid metabolism. Annu. Rev. Nutr. 4: 409 -454.
  20. Ahlborg, G., Felig, P., Hagenfeldt, L., Hendler, R. & Wahren, J. (1974) Substrate turnover during prolonged exercise in man. J. Clin. Invest. 53: 1080 - 1090.
  21. Ruberman, N. B. (1975) Muscle amino acid metabolism and gluco- neogenesis. Ann. Rev. Med. 26: 245-258.
  22. Patti, M.-E., Brambilla, E., Luzi, L., Landaker, E. J. & Kahn, C. R. (1998) Bidirectional modulation of insulin action by amino acids. J. Clin. Invest. 101: 1519 -1529.
  23. Xu, G., Kwon, G., Marshall, C. A., Lin, T.-A. & Lawrence, J. C. (1998)
  24. Branched-chain amino acids are essential in the regulation of PHAS-I and p70 S6 kinase by pancreatic ␤-cells. J. Biol. Chem. 273: 28178 -28184.
  25. Anthony, J. C., Anthony, T. G., Kimball, S. R. & Jefferson, L. S. (2001) Signaling pathways involved in translational control of protein synthesis in skeletal muscle by leucine. J. Nutr. 131: 856S-860S.
  26. Tischler, M. E., Desautels, M. & Goldberg, A. L. (1982) Does leucine, leucyl-tRNA, or some metabolite of leucine regulate protein synthesis in degra- dation in skeletal and cardiac muscle? J. Biol. Chem. 257: 1613-1621. 25. FAO/WHO/UNU. (1985) Energy and protein requirements. Report of joint FAO/WHO/UNU expert consultation. WHO Tech. Pep. Ser. 724: 1-206.
  27. Anthony, J. C., Yoshizawa, F., Gautsch-Anthony, T., Vary, T. C., Jeffer- son, L. S. & Kimball, S. R. (2000) Leucine stimulates translation initiation in skeletal muscle of postabsorptive rats via a rapamycin-sensitive pathway. J. Nutr. 130: 2413-2419.
  28. El-Khoury, A. E., Kukagawa, N. K., Sanchez, M., Tsay, R. H., Gleason, R. E., Chapman, T. E. & Young, V. R. (1994) The 24-h pattern and rate of leucine oxidation, with particular reference to tracer estimates of leucine require- ments in healthy adults. Am. J. Clin. Nutr. 59: 1012-1020.
  29. Evans, W. J., Fisher, E. C., Hoerr, R. A. & Young, V. R. (1983) Protein metabolism and endurance exercise. Physician Sports Med. 11: 63-72.
  30. Jungas, R. L., Halperin, M. L. & Brosnan, J. T. (1992) Quantitative analysis of amino acid oxidation and related gluconeogenesis in humans. Physiol. Rev. 72: 419 -448.
  31. Katz, J. & Tayek, J. A. (1998) Gluconeogenesis and the Cori cycle in 12-, 20-and 40-h-fasted humans. Am. J. Physiol. Endocrinol. Metab. 38: E537- E542.
  32. Balasubramanyam, A., McKay, S., Nadkarni, P., Rajan, A. S., Farza, A., Pavlik, V., Herd, J. A., Jahoor, F. & Reeds, P. J. (1999) Ethnicity affects the postprandial regulation of glycogenolysis. Am. J. Physiol. Endocrinol. Metab. 40: E905-E914.
  33. Fulks, R. M., Li, J. B. & Goldberg, A. L. (1975) Effects of insulin, glucose, and amino acids on protein turnover in rat diaphragm. J. Biol. Chem. 250: 290 -298.
  34. Li, J. B. & Jefferson, L. S. (1978) Influence of amino acid availability on protein turnover in perfused skeletal muscle. Biochim. Biophys. Acta 544: 351- 359.
  35. Hong, S. C. & Layman, D. K. (1984) Effects of leucine on in vitro protein synthesis and degradation in rat skeletal muscle. J. Nutr. 114: 1204 -1212.
  36. Anthony, J. C., Gautsch-Anthony, T. & Layman, D. K. (1999) Leucine supplementation enhances skeletal muscle recovery in rats following exercise. J. Nutr. 129: 1102-1106.
  37. Tipton, K. D., Ferrando, A. A., Phillips, S. M., Doyle, D. & Wolfe, R. R. (1999) Postexercise net protein synthesis in human muscle from orally admin- istered amino acids. Am. J. Physiol. Endocrinol. Metab. 276: E628 -E634.
  38. Anthony, J. C., Gautsch Anthony, T., Kimball, S. R., Vary, T. C. & Jeffer- son, L. S. (2000) Orally administered leucine stimulates protein synthesis in skeletal muscle of postabsorptive rats in association with increased eIF4F for- mation. J. Nutr. 130: 139 -145.
  39. Gautsch, T. A., Anthony, J. C., Kimball, S. R., Paul, G. L., Layman, D. K.
  40. & Jefferson, L. S. (1998) Availability of eIF4E regulates skeletal muscle protein synthesis during recovery from exercise. Am. J. Physiol. Cell Physiol. 274: C406 - C414.
  41. Anthony, J. C., Anthony, T. G., Kimball, S. R. & Jefferson, L. S. (2001) Signaling pathways involved in translational control of protein synthesis in skeletal muscle by leucine. J. Nutr. 131: 856S-860S.
  42. Food and Nutrition Board. (1989) Recommended Dietary Allowances, 10th ed. National Academy Press, Washington, D.C.
  43. Mayer, J. (1972) Dietary controls of diabetes. In: Human Nutrition: Its Physiological, Medical and Social Aspects, pp. 525-535. Charles C Thomas, Springfield, IL.
  44. Layman, D. K., Boileau, R., Painter, J., Erickson, D., Shiue, H. & Sather, C. (2000) Carbohydrates versus protein in diets for mid-life women. FASEB J. 14: A564 (abs.).
  45. Baum, J., Layman, D., Erickson, D., Boileau, R., Painter, J., Shiue, H. & Sather, C. (2002) Increased dietary protein alters glucose homeostasis during weight loss. FASEB J. 16: A260 (abs.).
  46. Layman, D. K., Shiue, H., Sather, C., Erickson, D. J. & Baum, J. (2003) Increased dietary protein modifies glucose and insulin homeostasis in adult women during weight loss. J. Nutr. (in press).
  47. Layman, D. K., Boileau, R. A., Erickson, D. J., Painter, J. E., Shiue, H., Sather, C. & Christou, D. D. (2003) A reduced ratio of dietary carbohydrate to protein improves body composition and blood lipid profiles during weight loss in adult women. J. Nutr. (in press).
  48. Skov, A. R., Toubro, S., Ronn, B., Holm, L. & Astrup, A. (1999) Ran- domized trial on protein vs carbohydrate in ad libitum fat reduced diet for the treatment of obesity. Int. J. Obes. 23: 528 -536.
  49. Mikkelsen, P. B., Toubro, S. & Astrup. A. (2000) Effect of fat-reduced diets on 24-h energy expenditure: comparisons between animal protein, vegeta- ble protein, and carbohydrate. Am. J. Clin. Nutr. 72: 1135-1141.
  50. Reeds, P. J., Burrin, D. G., Davis, T. A. & Stoll, B. (1998) Amino acid metabolism and the energetics of growth. Arch. Anim. Nutr. 51: 187-197.
  51. Nuttall, F. Q., Mooradian, A. D., Gannon, M. C., Billington, C. J. & Krezowski, P. A. (1984) Effect of protein ingestion on the glucose and insulin response to a standardized oral glucose load. Diabetes Care 7: 465-470.
  52. Ferrannini, E., Bevilacqua, S., Lanzone, L., Bonadonna, R., Brandi, L., Oleggini, M., Boni, C., Buzzigoli, G., Ciociaro, D., Luzi, L. & DeFronzo, R. A. (1988) Metabolic interactions of amino acids and glucose in healthy humans. Diabet. Nutr. Metab. 3: 175-186.
  53. Reaven, G. M. (1993) Role of insulin resistance in human disease (Syndrome X): an expanded definition. Ann. Rev. Med. 44: 121-131.
  54. Kabir, M., Rizkalla, S. W., Quignard-Boulange, A., Guerre-Millo, M., Boil- lot, J., Ardouin, B., Luo, J. & Slama, G. (1998) A high glycemic index starch diet affects lipid storage-related enzymes in normal and to a lesser extent in diabetic rats. J. Nutr. 128: 1878 -1883.
  55. Bistrian, B. R., Winterer, J., Blackburn, G. L., Young, V. & Sherman, M. (1977) Effect of a protein-sparing diet and brief fast on nitrogen metabolism in mildly obese subjects. J. Lab. Clin. Med. 89: 1030 -1035.
  56. Fafournoux, P., Remesy, C. & Demigne, C. (1983) Control of alanine metabolism in rat liver by transport processes or cellular metabolism. Biochem. J. 210: 645-652.
  57. Wagenmakers, A.J.M. (1999) Muscle amino acid metabolism at rest and during exercise: role in human physiology and metabolism. Diabet. Nutr. Metab. 12: 316 -322.
  58. Crapo, P. A., Reaven, G. & Olefsky, J. (1976) Plasma glucose and insulin responses to orally administered simple and complex carbohydrates. Diabetes 25: 741-747.
  59. Shapiro, E. T., Tillil, H., Miller, M. A., Frank, B. H., Galloway, J. A., Rubenstein, A. H. & Polonsky, K. S. (1987) Insulin secretion and clearance: comparison after oral and intravenous glucose. Diabetes 36: 1365-1371.
  60. Poortmans, J. R. & Dellalieux, O. (2000) Do regular high protein diets have potential health risks on kidney function in athletes? Int. J. Sport Nutr. Exerc. Metab. 10: 28 -38.
  61. Brenner, B. M., Meyer, T. W. & Hostetter, T. H. (1982) Dietary protein intake and the progressive nature of kidney disease. N. Engl. J. Med. 307: 652-659.
  62. Addis, T. (1948) Glomerular Nephritis: Diagnosis and Treatment. Mac- millan, New York, NY.
  63. Brandle, E., Sieberth, H. G. & Hautmann, R. E. (1996) Effect of chronic dietary protein intake on the renal function in healthy subjects. Eur. J. Clin. Nutr. 50: 734 -740.
  64. Rudman, D., DiFulco, T. J., Galambos, J. T., Smith, R. B., Salam, A. A. & Warren, W. D. (1973) Maximal rates of excretion and synthesis of urea in normal and cirrhotic subjects. J. Clin. Invest. 52: 2241-2249.