Hostname: page-component-cd9895bd7-7cvxr Total loading time: 0 Render date: 2024-12-31T15:28:20.244Z Has data issue: false hasContentIssue false
  • English
  • Français

Amino acids and insulin are regulators of muscle protein synthesis in neonatal pigs

Published online by Cambridge University Press:  21 May 2010

T. A. Davis ,
A. Suryawan ,
R. A. Orellana ,
M. L. Fiorotto  and
D. G. Burrin
T. A. Davis*
Affiliation:
United States Department of Agriculture/Agriculture Research Service Children’s Nutrition Research Center, Baylor College of Medicine, Houston, TX 77030, USA
A. Suryawan
Affiliation:
United States Department of Agriculture/Agriculture Research Service Children’s Nutrition Research Center, Baylor College of Medicine, Houston, TX 77030, USA
R. A. Orellana
Affiliation:
United States Department of Agriculture/Agriculture Research Service Children’s Nutrition Research Center, Baylor College of Medicine, Houston, TX 77030, USA
M. L. Fiorotto
Affiliation:
United States Department of Agriculture/Agriculture Research Service Children’s Nutrition Research Center, Baylor College of Medicine, Houston, TX 77030, USA
D. G. Burrin
Affiliation:
United States Department of Agriculture/Agriculture Research Service Children’s Nutrition Research Center, Baylor College of Medicine, Houston, TX 77030, USA
*
†E-mail: [email protected]
Get access

Abstract

The stage of development between birth and weaning in mammals is a period of very rapid growth that is crucial for the long-term well-being of the animal. The rate of protein deposition in neonatal animals is very high because dietary protein is efficiently utilized to increase body protein mass. Our studies in neonatal pigs have shown that this high efficiency of protein deposition is largely due to the marked increase in protein synthesis after feeding, and this response is particularly profound in the skeletal muscle. The enhanced stimulation of muscle protein synthesis in neonates after feeding is independently mediated by the rise in insulin and amino acids and this response declines with age. Intracellular signaling components that respond to the postprandial rise in amino acids and insulin have been identified and their activation has been shown to be elevated in skeletal muscle of neonatal pigs after a meal and to decrease with development. The enhanced activation of these components in the amino acid and insulin signaling pathways in neonatal muscle contributes to the high rate of muscle protein synthesis and rapid gain in skeletal muscle mass in newborn pigs, which are essential determinants of efficient growth during development.

Keywords

growthnewbornprotein metabolismtranslation initiationmammalian target of rapamycin
Type
EAAP-ASAS-ADSA Growth and Development Symposium 2008
Information
animal , Volume 4 , Issue 11 , November 2010 , pp. 1790 - 1796
Copyright
Copyright © The Animal Consortium 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Avruch, J, Lin, Y, Long, X, Murthy, S, Ortiz-Vega, S 2005. Recent advances in the regulation of the TOR pathway by insulin and amino acids. Current Opinion in Clinical Nutrition and Metabolic Care 8, 67–72.Google Scholar
Baillie, AG, Garlick, PJ 1992. Attenuated responses of muscle protein synthesis to fasting and insulin in adult female rats. American Journal of Physiology 262, E1–E5.Google ScholarPubMed
Bennet, WM, Connacher, AA, Scrimgeour, CM, Rennie, MJ 1990. The effect of amino acid infusion on leg protein turnover assessed by L-[15N]phenylalanine and L-[1-13C]leucine exchange. European Journal of Clinical Investigation 20, 41–50.Google Scholar
Bevan, P 2001. Insulin signalling. Journal of Cell Science 114, 1429–1430.CrossRefGoogle ScholarPubMed
Burrin, DG, Davis, TA, Ebner, S, Schoknecht, PA, Fiorotto, ML, Reeds, PJ, McAvoy, S 1995. Nutrient-independent and nutrient-dependent factors stimulate protein synthesis in colostrum-fed newborn pigs. Pediatric Research 37, 593–599.CrossRefGoogle ScholarPubMed
Davis, TA, Fiorotto, ML, Reeds, PJ 1993a. Amino acid compositions of body and milk protein change during the suckling period in rats. Journal of Nutrition 123, 947–956.CrossRefGoogle ScholarPubMed
Davis, TA, Fiorotto, ML, Nguyen, HV, Reeds, PJ 1993b. Enhanced response of muscle protein synthesis and plasma insulin to food intake in suckled rats. American Journal of Physiology 265, R334–R340.Google Scholar
Davis, TA, Fiorotto, ML, Nguyen, HV, Reeds, PJ 1989. Protein turnover in skeletal muscle of suckling rats. American Journal of Physiology 257, R1141–R1146.Google Scholar
Davis, TA, Burrin, DG, Fiorotto, ML, Nguyen, HV 1996. Protein synthesis in skeletal muscle and jejunum is more responsive to feeding in 7- than 26-day-old pigs. American Journal of Physiology 270, E802–E809.Google Scholar
Davis, TA, Nguyen, HV, Suryawan, A, Bush, JA, Jefferson, LS, Kimball, SR 2000. Developmental changes in the feeding-induced stimulation of translation initiation in muscle of neonatal pigs. American Journal of Physiology – Endocrinology and Metabolism 279, E1226–E1234.Google Scholar
Davis, TA, Fiorotto, ML, Beckett, PR, Burrin, DG, Reeds, PJ, Wray-Cahen, D, Nguyen, HV 2001. Differential effects of insulin on peripheral and visceral tissue protein synthesis in neonatal pigs. American Journal of Physiology – Endocrinology and Metabolism 280, E770–E779.Google Scholar
Davis, TA, Fiorotto, ML, Burrin, DG, Reeds, PJ, Nguyen, HV, Beckett, PR, Vann, RC, O’Connor, PM 2002. Stimulation of protein synthesis by both insulin and amino acids is unique to skeletal muscle in neonatal pigs. American Journal of Physiology – Endocrinology and Metabolism 282, E880–E890.Google Scholar
Denne, SC, Rossi, EM, Kalhan, SC 1991. Leucine kinetics during feeding in normal newborns. Pediatric Research 30, 23–27.CrossRefGoogle ScholarPubMed
Di Guglielmo, GM, Drake, PG, Baass, PC, Authier, F, Posner, BI, Bergeron, JJ 1998. Insulin receptor internalization and signaling. Molecular and Cellular Biochemistry 182, 59–63.CrossRefGoogle Scholar
Egawa, K, Sharma, PM, Nakashima, N, Huang, Y, Huver, E, Boss, GR, Olefsky, JM 1999. Membrane-targeted phosphatidylinositol 3-kinase mimics insulin actions and induces a state of cellular insulin resistance. Journal of Biological Chemistry 274, 14306–14314.Google Scholar
Egawa, K, Maegawa, H, Shimizu, S, Morino, K, Nishio, Y, Bryer-Ash, M, Cheung, AT, Kolls, JK, Kikkawa, R, Kashiwagi, A 2001. Protein-tyrosine phosphatase-1B negatively regulates insulin signaling in L6 myocytes and Fao hepatoma cells. Journal of Biological Chemistry 276, 10207–10211.CrossRefGoogle ScholarPubMed
Escobar, J, Frank, JW, Suryawan, A, Nguyen, HV, Kimball, SR, Jefferson, LS, Davis, TA 2005. Physiological rise in plasma leucine stimulates muscle protein synthesis in neonatal pigs by enhancing translation initiation factor activation. American Journal of Physiology – Endocrinology and Metabolism 288, E914–E921.CrossRefGoogle ScholarPubMed
Escobar, J, Frank, JW, Suryawan, A, Nguyen, HV, Kimball, SR, Jefferson, LS, Davis, TA 2006. Regulation of cardiac and skeletal muscle protein synthesis by individual branched-chain amino acids in neonatal pigs. American Journal of Physiology – Endocrinology and Metabolism 290, E612–E621.Google Scholar
Fiorotto, ML, Davis, TA, Reeds, PJ 2000. Regulation of myofibrillar protein turnover during maturation in normal and undernourished rat pups. American Journal of Physiology – Regulatory, Integrative and Comparative Physiology 278, R845–R854.Google Scholar
Garlick, PJ, Fern, M, Preedy, VR 1983. The effect of insulin infusion and food intake on muscle protein synthesis in postabsorptive rats. Biochemical Journal 210, 669–676.CrossRefGoogle ScholarPubMed
Gelfand, RA, Barrett, EJ 1987. Effect of physiologic hyperinsulinemia on skeletal muscle protein synthesis and breakdown in man. Journal of Clinical Investigation 80, 1–6.Google Scholar
Goberdhan, DC, Wilson, C 2003. PTEN: tumour suppressor, multifunctional growth regulator and more. Human Molecular Genetics 12, R239–R248.Google Scholar
Hara, K, Maruki, Y, Long, X, Yoshino, K, Oshiro, N, Hidayat, S, Tokunaga, C, Avruch, J, Yonezawa, K 2002. Raptor, a binding partner of target of rapamycin (TOR), mediates TOR action. Cell 110, 177–189.CrossRefGoogle ScholarPubMed
Hardie, DG 2005. New roles for the LKB1–AMPK pathway. Current Opinion in Cell Biology 17, 167–173.CrossRefGoogle ScholarPubMed
Harmon, CS, Proud, CB, Pain, VM 1984. Effects of starvation, diabetes, and acute insulin treatment on the regulation of polypeptide-chain initiation in rat skeletal muscle. Biochemical Journal 223, 687–696.Google Scholar
Inoki, K, Zhu, T, Guan, KL 2003. TSC2 mediates cellular energy response to control cell growth and survival. Cell 115, 577–590.CrossRefGoogle ScholarPubMed
Kelly, F, Lewis, SEM, Anderson, P, Goldspink, DF 1984. Pre- and postnatal growth and protein turnover in four muscles of the rat. Muscle and Nerve 7, 235–242.Google Scholar
Kim, DH, Sarbassov, DD, Ali, SM, King, JE, Latek, RR, Erdjument-Bromage, H, Tempst, P, Sabatini, DM 2002. mTOR interacts with raptor to form a amino acid-sensitive complex that signals to the cell growth machinery. Cell 110, 163–175.CrossRefGoogle Scholar
Kimball, SR 2007. The role of nutrition in stimulating muscle protein accretion at the molecular level. Biochemical Society Transactions 35, 1298–1301.Google Scholar
Kimball, SR, Jefferson, LS 2006. New functions for amino acids: effects on gene transcription and translation. American Journal of Clinical Nutrition 83, 500S–507S.CrossRefGoogle ScholarPubMed
Kimball, SR, Farrell, PA, Nguyen, HV, Jefferson, LS, Davis, TA 2002. Developmental decline in components of signal transduction pathways regulating protein synthesis in pig muscle. American Journal of Physiology – Endocrinology and Metabolism 282, E585–E592.Google Scholar
Kwiatkowski, DJ, Manning, BD 2005. Tuberous sclerosis: a GAP at the crossroads of multiple signaling pathways. Human Molecular Genetics 14, R251–R258.CrossRefGoogle ScholarPubMed
Liechty, EA, Boyle, DW, Moorehead, H, Liu, YM, Denne, SC 1992. Effect of hyperinsulinemia on ovine fetal leucine kinetics during prolonged maternal fasting. American Journal of Physiology 263, E696–E702.Google Scholar
Long, X, Ortiz-Vega, S, Lin, Y, Avruch, J 2005. Rheb binding to mammalian target of rapamycin (mTOR) is regulated by amino acid sufficiency. Journal of Biological Chemistry 280, 23433–23436.CrossRefGoogle ScholarPubMed
Martin, DE, Hall, MN 2005. The expanding TOR signaling network. Current Opinions in Cell Biology 17, 158–166.CrossRefGoogle ScholarPubMed
Melville, S, McNurlan, MA, McHardy, KC, Broom, J, Milne, E, Calder, AG, Garlick, PJ 1989. The role of degradation in the acute control of protein balance in adult man: failure of feeding to stimulate protein synthesis as assessed by L-[1-13C]leucine infusion. Metabolism: Clinical and Experimental 38, 248–255.Google Scholar
Niedzwiecka, A, Stepinski, J, Darzynkiewicz, E, Conenberg, N, Stolarski, R 2002. Positive heat capacity change upon specific binding of translation initiation factor eIF4E to mRNA 5’cap. Biochemistry 41, 12140–12148.Google Scholar
O’Connor, PM, Bush, JA, Suryawan, A, Nguyen, HV, Davis, TA 2003a. Insulin and amino acids independently stimulate skeletal muscle protein synthesis in neonatal pigs. American Journal of Physiology – Endocrinology and Metabolism 284, E110–E119.Google Scholar
O’Connor, PM, Kimball, SR, Suryawan, A, Bush, JA, Nguyen, HV, Jefferson, LS, Davis, TA 2003b. Regulation of translation initiation by insulin and amino acids in skeletal muscle of neonatal pigs. American Journal of Physiology – Endocrinology and Metabolism 285, E40–E53.CrossRefGoogle ScholarPubMed
O’Connor, PM, Kimball, SR, Suryawan, A, Bush, JA, Nguyen, HV, Jefferson, LS, Davis, TA 2004. Regulation of neonatal liver protein synthesis by insulin and amino acids in pigs. American Journal of Physiology – Endocrinology and Metabolism 286, E994–E1003.Google Scholar
Oddy, VH, Lindsay, DB, Barker, PJ, Northrop, AJ 1987. Effect of insulin on hindlimb and whole body leucine and protein metabolism in fed and fasted lambs. British Journal of Nutrition 58, 437–452.Google Scholar
Peterson, RT, Desai, BN, Hardwick, JS, Schreiber, SL 1999. Protein phosphatase 2A interacts with the 70-kDa S6 kinase and is activated by inhibition of FKBP12-rapamycin associated protein. Proceedings of the National Academy of Sciences of the United States of America 96, 4438–4442.CrossRefGoogle Scholar
Preedy, VR, Garlick, PJ 1986. The response of muscle protein synthesis to nutrient intake in postabsorptive rats: the role of insulin and amino acids. Bioscience Reports 6, 177–183.Google Scholar
Proud, CG 2004. Role of mTOR signalling in the control of translation initiation and elongation by nutrients. Current Topics in Microbiology and Immunology 279, 215–244.Google ScholarPubMed
Reeds, PJ, Fiorotto, ML, Davis, TA, Burrin, DG 1992. Homeorrhesis and homeostasis: problems of growth and maintenance. In Frontiers and New Horizons in Amino Acid Research (ed. K Takai), pp. 133–144. Elsevier Science Publishers, Amsterdam, The Netherlands.Google Scholar
Reeds, PJ, Burrin, DG, Davis, TA, Fiorotto, ML 1993. Postnatal growth of gut and muscle: competitors or collaborators? Proceedings of the Nutrition Society 52, 57–67.Google Scholar
Sabitini, DM 2006. mTOR and cancer: insights into a complex relationship. Nature Reviews Cancer 6, 729–734.CrossRefGoogle Scholar
Smith, EM, Finn, SG, Tee, AR, Browne, GJ, Proud, CG 2005. The tuberous sclerosis protein TSC2 is not required for the regulation of the mammalian target of rapamycin by amino acids and certain cellular stresses. Journal of Biological Chemistry 280, 18717–18727.CrossRefGoogle Scholar
Suryawan, A, Davis, TA 2003. Protein-tyrosine-phosphatase 1B activation is regulated developmentally in muscle of neonatal pigs. American Journal of Physiology – Endocrinology and Metabolism 284, E47–E54.Google Scholar
Suryawan, A, Davis, TA 2005. Developmental regulation of protein kinase B activation is isoform specific in skeletal muscle of neonatal pigs. Pediatric Research 58, 719–724.Google Scholar
Suryawan, A, Nguyen, HV, Bush, JA, Davis, TA 2001. Developmental changes in the feeding-induced activation of the insulin-signaling pathway in neonatal pigs. American Journal of Physiology – Endocrinology and Metabolism 281, E908–E915.Google Scholar
Suryawan, A, Escobar, J, Frank, JW, Nguyen, HV, Davis, TA 2006. Developmental regulation of the activation of signaling components leading to translation initiation in skeletal muscle of neonatal pigs. American Journal of Physiology – Endocrinology and Metabolism 291, E849–E859.CrossRefGoogle ScholarPubMed
Suryawan, A, O’Connor, PM, Bush, JA, Nguyen, HV, Davis, TA 2009. Differential regulation of protein synthesis by amino acids and insulin in peripheral and visceral tissues of neonatal pigs. Amino Acids 37, 97–104.Google Scholar
Suryawan, A, Orellana, RA, Nguyen, HV, Jeyapalan, AS, Fleming, JR, Davis, TA 2007. Activation by insulin and amino acids of signaling components leading to translation initiation in skeletal muscle of neonatal pigs is developmentally regulated. American Journal of Physiology – Endocrinology and Metabolism 293, E1597–E1605.Google Scholar
Suryawan, A, O’Connor, PM, Kimball, SR, Bush, JA, Nguyen, HV, Jefferson, LS, Davis, TA 2004. Amino acids do not alter the insulin-induced activation of the insulin signaling pathway in neonatal pigs. Journal of Nutrition 134, 24–30.Google Scholar
Vann, RC, Nguyen, HV, Reeds, PJ, Steele, NC, Deaver, DR, Davis, TA 2000. Somatotropin increases protein balance independent of insulin’s effects on protein metabolism in growing pigs. American Journal of Physiology – Endocrinology and Metabolism 279, E1–E10.Google Scholar
Volpi, E, Ferrando, AA, Yeckel, CW, Tipton, KD, Wolfe, RR 1998. Exogenous amino acids stimulate net muscle protein synthesis in the elderly. Journal of Clinical Investigation 101, 2000–2007.CrossRefGoogle ScholarPubMed
Wester, TJ, Lobley, GE, Birnie, LM, Lomax, MA 2000. Insulin stimulates phenylalanine uptake across the hind limb in fed lambs. Journal of Nutrition 130, 608–611.Google Scholar
White, MF, Kahn, CR 1994. The insulin-signaling system. Journal of Biological Chemistry 269, 1–4.Google Scholar
Wray-Cahen, D, Beckett, PR, Nguyen, HV, Davis, TA 1997. Insulin-stimulated amino acid utilization during glucose and amino acid clamps decreases with development. American Journal of Physiology 273, E305–E314.Google Scholar
Wray-Cahen, D, Nguyen, HV, Burrin, DG, Beckett, PR, Fiorotto, ML, Reeds, PJ, Wester, TJ, Davis, TA 1998. Response of skeletal muscle protein synthesis to insulin in suckling pigs decreases with development. American Journal of Physiology 275, E602–E609.Google ScholarPubMed
Young, VR 1970. The role of skeletal and cardiac muscle in the regulation of protein metabolism. In Mammalian Protein Metabolism (ed. HM Munro), pp. 585–674. Academic Press, New York, NY, USA.CrossRefGoogle Scholar