Interaction of amino acids and insulin in the regulation of protein metabolism in growing animals

Canadian Journal of Animal Science

Volumn 83, Issue 3, 2003, Pages 357-364

  Davis, T A ^a   Suryawan, A ^a   Bush, J A ^a   O'Connor, P M J ^a   Thivierge, M C ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Amino acids; Insulin; Muscle; Neonate; Pigs; Protein synthesis

Indexed keywords

ANIMALIA;

EID: 0345107261     PISSN: 00083984     EISSN: None     Source Type: Journal    
DOI: 10.4141/A02-120     Document Type: Review

References (71)

1. Backer, J. M., Myers, M. G., Shoelson, S. E., Chin, D. J., Sun, X. J., Miralpeix, M., Hu, P., Margolis, B., Skolnik, E. Y. and Schlessinger, J. 1992. Phosphatidylinositol 3-kinase is activated by association with IRS-1 during insulin stimulation. EMBO J. 11: 3469-3479.
2. Baillie, A. G. S. and Garlick, P. J. 1992. Attenuated responses of muscle protein synthesis to fasting and insulin in adult female rats. Am. J. Physiol. Endocrinol. Metab. 262: E1-E5.
3. Bennet, W. M., Connacher, A. A., Scrimgeour, C. M. and Rennie, M. J. 1990. The effect of amino acid infusion on leg protein turnover assessed by L-[15N] phenylalanine and L-[1-13C]leucine exchange. Cur. J. Clin. Invest. 20: 41-50.
4. Burrin, D. G., Davis, T. A., Ebner, S., Schoknecht, P. A., Fiorotto, M. L. and Reeds, P. J. 1997. Colostrum enhances the nutritional stimulation of vital organ protein synthesis in neonatal pigs. J. Nutr. 127: 1284-1289.
5. Burrin, D. G., Davis, T. A., Ebner, S., Schoknecht, P. A., Fiorotto, M. L., Reeds, P. J. and McAvoy, S. 1995. Nutrient-independent and nutrient-dependent factors stimulate protein synthesis in colostrum-fed newborn pigs. Pediatr. Res. 37: 593-599.
6. Burrin, D. G., Davis, T. A., Fiorotto, M. L. and Reeds, P. J. 1991. Stage of development and fasting affect protein synthetic activity in the gastrointestinal tissues of suckling rats. J. Nutr. 121:1099-1108.
7. Burrin, D. G., Davis, T. A., Fiorotto, M. L. and Reeds, P. J. 1992. Hepatic protein synthesis in suckling rats: effects of stage of development and fasting. Pediatr. Res. 31: 247-252.
8. Davis, T. A., Burrin, D. G., Fiorotto, M. L. and Nguyen, H. V. 1996. Protein synthesis in skeletal muscle and jejunum is more responsive to feeding in 7-than in 26-day-old pigs. Am. J. Physiol. Endocrinol. Metab. 270: E802-E809.
9. Davis, T. A., Fiorotto, M. L., Burrin, D. G., Pond, W. G. and Nguyen, H. V. 1997. Intrauterine growth restriction does not alter response of protein synthesis to feeding in newborn pigs. Am. J. Physiol. Endocrinol. Metab. 272: E877-E884.
10. Davis, T. A., Burrin, D. G., Fiorotto, M. L., Reeds, P. J. and Jahoor, F. 1998. Roles of insulin and amino acids in the regulation of protein synthesis in the neonate. J. Nutr. 128: 347S-350S.
11. Davis, T. A., Fiorotto, M. L., Burrin, D. G., Reeds, P. J., Nguyen, H. V., Beckett, P. R., Vann, R. C. and O'Connor, P. M. J. 2002. Stimulation of protein synthesis by both insulin and amino acids is unique to skeletal muscle in neonatal pigs. Am. J. Physiol. Endocrinol. Metab. 282: E880-E890.
12. Davis, T. A., Fiorotto, M. L., Nguyen, H. V. and Burrin, D. G. 1999. Aminoacyl-tRNA and tissue free amino acid pools are equilibrated after a flooding dose of phenylalanine. Am. J. Physiol. Endocrinol. Metab. 277: E103-E109.
13. Davis, T. A., Fiorotto, M. L., Nguyen, H. V., Burrin, D. G. and Reeds, P. J. 1991. Response of muscle protein synthesis to fasting in suckling and weaned rats. Am. J. Physiol. Regulatory Integrative Comp. Physiol. 261: R1373-1380.
14. Davis, T. A., Fiorotto, M. L., Nguyen, H. V. and Reeds, P. J. 1989. Protein turnover in skeletal muscle of suckling rats. Am. J. Physiol. Regulatory Integrative Comp. Physiol. 257: R1141-R1146.
15. Davis, T. A., Fiorotto, M. L., Nguyen, H. V. and Reeds, P. J. 1993a. Enhanced response of muscle protein synthesis and plasma insulin to food intake in suckled rats. Am. J. Physiol. Regulatory Integrative Comp. Physiol. 265: R334-R340.
16. Davis, T. A., Fiorotto, M. L. and Reeds, P. J. 1993b. Amino acid compositions of body and milk protein change during the suckling period in rats. J. Nutr. 123: 947-956.
17. Davis, T. A., Nguyen, H. V., Suryawan, A., Bush, J. A., Jefferson, L. S. and Kimball, L. S. 2000. Developmental changes in the feeding-induced stimulation of translation initiation in skeletal muscle and liver of neonatal pigs. Am. J. Physiol. Endocrinol. Metab. 279: E1226-E1234.
18. Davis, T. A., Fiorotto, M. L., Beckett, P. R., Burrin, D. G., Reeds, P. J., Wray-Cahen, D. and Nguyen, H. V. 2001. Differential effects of insulin on peripheral and visceral tissue protein synthesis in neonatal pigs. Am. J. Physiol. Endocrinol. Metab. 280: E770-E779.
19. DeFronzo, R. A., Tobin, J. D. and Andres, R. 1979. Glucose clamp technique: a method for quantifying insulin secretion and resistance. Am. J. Physiol. Endocrinol. Metab. 237: E214-E223.
20. Denne, S. C. and Kalhan, S. C. 1987. Leucine metabolism in human newborns. Am. J. Physiol. Endocrinol. Metab. 253: E608-E615.
21. Denne, S. C., Rossi, E. M. and Kalhan, S. C. 1991. Leucine kinetics during feeding in normal newborns. Pediatr. Res. 30: 23-27.
22. Dennis, P. B., Fumagalli, S. and Thomas, G. 1999. Target of rapamycin (TOR): balancing the opposing forces of protein synthesis and degradation. Curr. Opinion Cell Reg. 9: 49-54.
23. Fiorotto, M. L., Burrin, D. G., Perez, M. and Reeds, P. J. 1991. Intake and use of milk nutrients by rat pups suckled in small, medium, or large litters. Am. J. Physiol. Regulatory Integrative Comp. Physiol. 260: R1104-R1113.
24. Fiorotto, M. L., Davis, T. A. and Reeds, P. J. 2000. Regulation of myofibrillar protein turnover during maturation in normal and undernourished rat pups. Am. J. Physiol. Regulatory Integrative Comp. Physiol. 278: R845-R854.
25. Flaim, K. E., Peavy, D. E., Everson, W. V. and Jefferson, L. S. 1982. The role of amino acids in the regulation of protein synthesis in perfused rat liver. J. Biol. Chem. 257: 2932-2938.
26. Flynn, A. and Proud, C. G. 1996. Insulin-stimulated phosphorylation of initiation factor 4E is mediated by the MAP kinase pathway. FEBS Lett. 389: 162-166.
27. Garlick, P. J., Fern, M. and Preedy, V. R. 1983. The effect of insulin infusion and food intake on muscle protein synthesis in postabsorptive rats. Biochem. J. 210:669-676.
28. Gelfand, R. A. and Barrett, E. J. 1987. Effect of physiologic hyperinsulinemia on skeletal muscle protein synthesis and breakdown in man. J. Clin. Invest. 80: 1-6.
29. Goldspink, D. F. and Kelly, F. J. 1984. Protein turnover and growth in the whole body, liver and kidney of the rat from the foetus to senility. Biochem. J. 217: 507-516.
30. Harmon, C. S., Proud, C. G. and Pain, V. M. 1984. Effects of starvation, diabetes and acute insulin treatment on the regulation of polypeptide-chain initiation in rat skeletal muscle. Biochem. J. 223: 687-696.
31. Heslin, M. J., Newman, E., Wolf, R. F., Pisters, P. W. T. and Brennan, M. F. 1992. Effect of hyperinsulinemia on whole body and skeletal muscle leucine carbon kinetics in humans. Am. J. Physiol. Endocrinol. Metab. 262: E911-E918.
32. Jefferies, H. B., Reinhard, C., Kozma, S. C. and Thomas, G. 1994. Rapamycin electively represses translation of the "polypyrimidine tract" mRNA family. Proc. Natl. Acad. Sci. USA 91: 4441-4445.
33. Kelly, F., Lewis, S. E. M., Anderson, P. and Goldspink, D. F. 1984. Pre-and postnatal growth and protein turnover in four muscles of the rat. Muscle Nerve 8: 235-242.
34. Kimball, S. R., Farrell, P. A., Nguyen, H.V., Jefferson, L. S. and Davis, T. A. 2002. Developmental decline in components of signal transduction pathways regulating protein synthesis in pig muscle. Am. J. Physiol. Endocrinol. Metab. 282: E585-E592.
35. Kimball, S. R. and Jefferson, L. S. 1988. Cellular mechanisms involved in the action of insulin on protein synthesis. Diabetes Metab. Rev. 4: 773-787.
36. Kimball, S. R., Jurasinski, C. V., Lawrence, J. C. and Jefferson, L. S. 1997. Insulin stimulates protein synthesis in skeletal muscle by enhancing the association of eIF4E and eIF4G. Am. J. Physiol. 272: C754-C759.
37. Kimball, S. R., Jefferson, L. S., Nguyen, H. V., Suryawan, A., Bush, J. A. and Davis, T. A. 2000. Feeding stimulates protein synthesis in muscle and liver of neonatal pig through an mTOR-dependent process. Am. J. Physiol. Endocrinol. Metab. 279: E1080-E1087.
38. Kimball, S. R., Mellor, H., Flowers, K. M. and Jefferson, L. S. 1996. Role of translation initiation factor eIF2B in the regulation of protein synthesis in mammalian cells. Prog. Nucleic Acid Res. 54: 165-196.
39. Kimball, S. R., Shantz, L. M., Horetsky, R. L. and Jefferson, L. S. 1999. Leucine regulates translation of specific mRNA in L6 myoblasts through mTOR-mediated changes in availability of eIF4E and phosphorylation of ribosomal protein S6. J. Biol. Chem. 274: 11647-11652.
40. Kimball, S. R., Vary, T. C. and Jefferson, L. S. 1994. Regulation of protein synthesis by insulin. Ann. Rev. Physiol. 56: 321-348.
41. Liechty, E. A., Boyle, D. W., Moorehead, H, Liu, Y. M. and Denne, S. C. 1992. Effect of hyperinsulinemia on ovine fetal leucine kinetics during prolonged maternal fasting. Am. J. Physiol. Endocrinol. Metab. 263: E696-E702.
42. Louard, R. J., Fryburg, D. A., Gelfand, R. A. and Barrett, E. J. 1992. Insulin sensitivity of protein and glucose metabolism in human forearm skeletal muscle. J. Clin. Invest. 90: 2348-2354.
43. McCracken, K. J., Eddie, S. M. and Stevenson, W. G. 1980. Energy and protein nutrition of early-weaned pigs. Effect of energy intake and energy: protein on growth, efficiency and nitrogen utilization of pigs between 8-32d. Br. J. Nutr. 43: 289-304.
44. McNulty, P. A., Young, L. H. and Barrett, E. J. 1993. Response of rat heart and skeletal muscle protein in vivo to insulin and amino acid infusion. Am. J. Physiol. Endocrinol. Metab. 264: E958-E965.
45. 13C]leucine infusion. Metabolism 38: 248-255.
46. Mosoni, L., Houlier, M.-L., Mirand, P. P., Bayle, G. and Grizard, J. 1993. Effect of amino acids alone or with insulin on muscle and liver protein synthesis in adult and old rats. Am. J. Physiol. 264: E614-0E620.
47. Mosoni, L., Malmezat, T., Valluy, M.-C., Houlier, M.-L. and Mirand, P. P. 1996. Muscle and liver protein synthesis adapt efficiently to food deprivation and refeeding in 12-month-old rats. J. Nutr. 126: 516-522.
48. Oddy, V. H., Lindsay, D. B., Barker, P. J. and Northrop, A. J. 1987. Effect of insulin on hind-limb and whole body leucine and protein metabolism in fed and fasted lambs. Br. J. Nutr. 58: 437-452.
49. Pain, V. M. 1996. Initiation of protein synthesis in eukaryotic cells. Eur. J. Biochem. 236: 747-771.
50. Pellett, P. L. and Kaba, H. 1972. Carcass amino acids of the rat under conditions of determination of net protein utilization. J. Nutr. 102: 61-68.
51. Preedy, V. T. and Garlick, P. J. 1986. The response of muscle protein synthesis to nutrient intake in postabsorptive rats: the role of insulin and amino acids. Biosci. Rep. 6: 177-183.
52. Preedy, V. T. and Garlick, P. J. 1993. Response of muscle protein synthesis to parenteral administration of amino acid mixtures in growing rats. J. Parenter. Enteral. Nutr. 17: 113-118.
53. Preedy, V. R., Paska, L., Sugden, P., Schofield, P. and Sugden, M. C. 1988. The effects of surgical stress and short-term fasting on protein synthesis in vivo in diverse tissues of the mature rat. Biochem. J. 250: 179-188.
54. Rhoads, R. E. 1994. Regulation of eukaryotic protein synthesis by initiation factors in the recruitment of mRNA to ribosomes. Biochimie 76: 831-838.
55. Scott, P. H., Brunn, G. J., Kohn, A. D., Roth, R. A. and Lawrence, J. C. 1998. Evidence of insulin-stimulated phosphorylation and activation of the mammalian target of rapamycin mediated by a protein kinase B signaling pathway. Proc. Natl. Acad. Sci. USA 95: 7772-7777.
56. Shah, O. J., Antonetti, D. A., Kimball, S. R. and Jefferson, L. S. 1999. Leucine, glutamine, and tyrosine reciprocally modulate the translation initiation factors eIF4F and eIF2B in perfused rat liver. J. Biol. Chem. 274: 36168-36175.
57. Skjaerlund, D. M., Mulvaney, D. R., Bergen, W. G. and Merkel, R. A. 1994. Skeletal muscle growth and protein turnover in neonatal boars and barrows. J. Anim. Sci. 72: 315-321.
58. Sonenberg, N. 1994. Regulation of translation and cell growth by eIF4E. Biochimie 76: 839-846.
59. Sun, X. J., Crimmins, D. L., Myers, M. G., Miralpeix, M. and White, M. F. 1993. Pleiotropic insulin signals are engaged by multisite phosphorylation of IRS-1. Mol. Cell Biol. 13: 7418-7428.
60. Sun, X. J., Rothenberg, P., Kahn, C. R., Backer, J. M., Araki, E., Cahill, P. A., Goldstein, B. J. and White, M. F. 1991. Structure of the insulin receptor substrate IRS-1 defines a unique signal transduction protein. Nature 352: 73-77.
61. Suryawan, A., Nguyen, H. V., Bush, J. A. and Davis, T.A. 2001. Developmental changes in the feeding-induced activation of the insulin signaling pathway in neonatal pigs. Am J Physiol. Endocrinol. Metab. 281: E908-E915.
62. Tessari, P., Zanetti, M., Barazzoni, R., Vettore, M. and Michielan, F. 1996. Mechanism of postprandial protein accretion in human skeletal muscle. J. Clin. Invest. 98: 1361-1372.
63. Thureen P. J., Scheer, B., Anderson, S. M., Tooze, J. A., Young, D. A. and Hay, W. W. 2000. Effect of hyperinsulinemia on amino acid utilization in the ovine fetus. Am. J. Physiol. Endocrinol. Metab. 279: E1294-E1304.
64. Vary, T. C., Jefferson, L. S. and Kimball, S. R., 1999. Amino acid-induced stimulation of translation initiation in rat skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 277: E1077-E1086.
65. Volpi, E., Ferando, A. A., Yeckel, C. W., Tipton, K. D. and Wolfe R. R. 1998. Exogenous amino acids stimulate net muscle protein synthesis in the elderly. J. Clin. Invest. 101: 2000-2007.
66. Von Manteuffel, S. R., Dennis, P. B., Pullen, N., Gingras, A. C., Sonenberg, N. and Thomas, G. 1997. The insulin-induced signaling pathway leading to S6 and initiation factor 4E binding protein 1 phosphorylation bifurcates at a rapamycin-sensitive point immediately upstream of p70S6K. Mol. Cell. Biol. 17: 5426-5436.
67. Wester, T. J., Lobley, G. E., Birnie, L. M. and Lomax, M. A. 2000. Insulin stimulates phenylalanine uptake across the hind limb in fed lambs. J. Nutr. 130: 608-611.
68. White, M. F. and Kahn, C. R. 1994. The insulin-signaling system. J. Biol. Chem. 269: 1-4.
69. Wray-Cahen, D., Beckett, P. R., Nguyen, H. V. and Davis, T. A. 1997. Insulin-stimulated amino acid utilization during glucose and amino acid clamps decreases with development. Am. J. Physiol. Endocrinol. Metab. 273: E305-E314.
70. Wray-Cahen, D., Nguyen, H. V., Burrin, D. G., Beckett, P. R., Fiorotto, M. L., Reeds, P. J., Wester, T. J. and Davis, T. A. 1998. Response of skeletal muscle protein synthesis to insulin in suckling pigs decreases with development. Am. J. Physiol. Endocrinol. Metab. 275: E602-E609.
71. Young, V. R. 1970. The role of skeletal and cardiac muscle in the regulation of protein metabolism. Pages 585-674 in H. M. Munro, ed. Mammalian protein metabolism. Vol. 4. Academic Press, New York, NY.