Nutrient signaling components controlling protein synthesis in striated muscle

Journal of Nutrition

Volumn 137, Issue 8, 2007, Pages 1835-1843

  Vary, Thomas C ^a   Lynch, Christopher J ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; ANABOLIC AGENT; INITIATION FACTOR 4E; INITIATION FACTOR 4G; LEUCINE; MAMMALIAN TARGET OF RAPAMYCIN; MESSENGER RNA; NITROGEN; PROTEIN; S6 KINASE;

HUMAN; MUSCLE MASS; NITROGEN BALANCE; NONHUMAN; NUTRIENT CONTENT; PROTEIN ASSEMBLY; PROTEIN INTAKE; PROTEIN RESTRICTION; PROTEIN SYNTHESIS; REFEEDING; REVIEW; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; TRANSLATION INITIATION; WASTING SYNDROME; WEIGHT REDUCTION;

ANIMALIA; EUKARYOTA; MAMMALIA;

EID: 34548074950     PISSN: 00223166     EISSN: 15416100     Source Type: Journal    
DOI: 10.1093/jn/137.8.1835     Document Type: Review

References (102)

1. Lynch CJ, Patson BJ, Anthony JC, Vaval A, Jefferson LS, Vary TC. Leucine is a direct acting nutrient signal that regulates protein synthesis in adipose tissue. Am J Physiol Endocrinol Metab. 2002;283:E824-35.
2. Yoshizawa F, Kimball SR, Vary TC, Jefferson LS. Effect of dietary protein on translation initiation in rat skeletal muscle and liver. Am J Physiol Endocrinol Metab. 1998;275:E814-20.
3. Garcia-de-Lorenzo A, Otiz-Leyba C, Planas M, Montejo JC, Numez R, Ordonez FJ, Aragon C, Jimenez FJ. Parental administration of different amount of branched-chain amino acids in septic patients: clinical and metabolic aspects. Crit Care Med. 1997;25:418-24.
4. Cerra FB, Mazuski JE, Chute E, Nuwer N, Teasley K, Lysne J, Shronts EP, Konstantinides FN. Branched chain metabolic support. A prospective, randomized, double-blind trial in surgical stress. Ann Surg. 1984;199:286-91.
5. Jimenez-Jimenez FJ, Ortiz-Leyba C, Morales-Menedez S, Barros-Perez M, Munoz-Gracia J. Prospective study on the efficacy of branched-chain amino acids in sepsis. JPEN J Parenter Enteral Nutr. 1991;15:252-61.
6. Choudry HA, Pan M, Karinch AM, Souba WW. Branched chain amino acid enriched nutritional support in surgical and cancer patients. J Nutr. 2006;136:S314-8.
7. Cooney RN, Kimball SR, Vary TC. Regulation of skeletal muscle protein turnover during sepsis: mechanisms and mediators. Shock. 1997;7:1-16.
8. Jefferson LS, Vary TC, Kimball SR. Regulation of protein metabolism in muscle. In: Jefferson LS, Cherrington AD, editors. Handbook of physiology. New York: Oxford University Press; 2001. p. 529-52.
9. Rieu I, Balage M, Sornet C, Giraudet C, Pujos E, Grizard J, Mosoni L, Dardevet D. Leucine supplementation improves muscle protein synthesis in elderly men independently of hyperaminoacidemia. J Physiol. 2006;575:305-15.
10. Anthony JC, Gautsch T, Kimball SR, Vary TC, Jefferson LS. Orally administered leucine stimulates protein synthesis in skeletal muscle of postabsorptive rats in association with increased eIF4F formation. J Nutr. 2000;130:139-45.
11. Vary TC, Jefferson LS, Kimball SR. Amino acid-induced stimulation of translation initiation in rat skeletal muscle. Am J Physiol Endocrinol Metab. 1999;277:E1077-86.
12. Rhoads RE, Joshi-Barve S, Minich WB. Participation of initiation factors in recruitment of mRNA to ribosomes. Biochimie. 1994;76:831-8.
13. Rhoads RE. Regulation of eukaryotic protein synthesis by initiation factors. J Biol Chem. 1993;268:3017-20.
14. Sonenberg N. Regulation of translation and cell growth by eIF-4E. Biochimie. 1994;76:839-46.
15. Balage M, Sinaud S, Prod'Homme M, Dardevet D, Vary TC, Kimball SR, Jefferson LS, Grizard J. Amino acids and insulin are both required to regulate assembly of eIF4E·eIF4G complex in rat skeletal muscle. Am J Physiol Endocrinol Metab. 2001;281:E565-74.
16. Lamphear BJ, Kirchweger JR, Skern T, Rhoads RE. Mapping of functional domains in eukaryotic protein synthesis initiation factor 4G (eIF-4G) with pircoviral proteases. Implication for cap-dependent and cap-independent translation initiation. J Biol Chem. 1995;270:21975-83.
17. Pyronnet S, Dostie J, Sonenberg N. Suppression of cap-dependent translation in mitosis. Genes Dev. 2001;15:2083-93.
18. Waskiewicz AJ, Flynn A, Proud CG, Cooper JA. Mitogen-activated protein kinases activate the serine/threonine kinases MNK1 and MNK2. EMBO J. 1997;16:1909-20.
19. Wells SE, Hillner PE, Vale RD, Sachs AB. Circularization of mRNA by eukaryotic translation initiation factors. Mol Cell. 1998;2:135-40.
20. Vary TC, Jefferson LS, Kimball SR. Insulin fails to stimulate muscle protein synthesis in sepsis despite unimpaired signaling to 4E-BP1 and S6K1. Am J Physiol Endocrinol Metab. 2001;281:E1045-53.
21. Lin T, Kong X, Haystead T, Pause A, Belsham G, Sonnenberg N, Lawrence J. PHAS-I as a link between mitogen activated protein kinase and translation initiation. Science. 1994;266:653-6.
22. Lin T, Kong X, Saltiel AR, Blackshear PJ, Lawrence JC. Control of PHAS-I by insulin in 3T3-L1 adipocytes. Synthesis, degradation, and phosphorylation by a rapamycin-sensitive and mitogen-activated protein kinase dependent pathway. J Biol Chem. 1995;270:18531-5.
23. Bhandari BK, Feliers D, Duraisamy S, Stewart JL, Gingas A-C, Abbound HE, Choudhury GG, Sonenberg N, Kasinath BS. Insulin regulation of protein translation repressor 4E-BP1, an eIF4E-binding protein in renal epithelial cells. Kidney Int. 2001;59:866-75.
24. Pause A, Belsham GJ, Gingras A-C, Donze O, Lin T-A, Lawrence JC Jr, Sonenberg N. Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5′-cap function. Nature. 1994;371:762-7.
25. Haghighat A, Mader S, Pause A, Sonenberg N. Repression of cap-dependent translation by 4E-binding protein I: competition with p220 for binding to eukaryotic initiation factor-4E. EMBO J. 1995;14:5701-9.
26. Avruch J. Insulin signal transduction through protein kinase cascades. Mol Cell Biochem. 1998;182:31-42.
27. Lynch CJ. Role of leucine in regulation of mTOR by amino acids: revelations from structure-activity studies. J Nutr. 2001;131:S861-5.
28. Kimball SR, Shantz LM, Horetsky RL, Jefferson LS. Leucine regulates translation of specific mRNAs in L6 myoblasts through mTOR mediated changes in availability of eIF4E and phosphorylation of ribosomal protein S6. J Biol Chem. 1999;274:11647-52.
29. Kozma SC, Thomas G. p70s6k/p85s6k: mechanism of activation and role in mitogenesis. Semin Cancer Biol. 1994;5:255-60.
30. Raught B, Gingras A-C, Gygi SP, Imaataka H, Morino S, Gradi A, Aebersold R, Sonenberg N. Serum-stimulated, rapamycin-sensitive phosphorylation sites in eukaryotic translation initiation factor 4GI. EMBO J. 2000;19:434-44.
31. Nguyen KA, Santos SJ, Kreidel MK, Diaz AL, Rey R, Lawson MA. Acute regulation of translation initiation by gonadotropin-releasing hormone in the gonadotrope cell line LβT2. Mol Endocrinol. 2004;18:1301-12.
32. Morley SJ, Traugh JA. Stimulation of translation in 3T3-L1 cells in response to insulin and phorbol ester is directly correlated with increased phosphate labeling of initiation factor (eIF-)4F and ribosomal protein S6. Biochimie. 1993;75:985-9.
33. Vary TC, Lynch CH. Meal feeding enhances formation of eIF4F in skeletal muscle: role of increased eIF4E availability and eIF4G phosphorylation. Am J Physiol Endocrinol Metab. 2006;290:E631-42.
34. Vary TC. IGF-I stimulates protein synthesis in skeletal muscle through multiple signaling pathways during sepsis. Am J Physiol Regul Integr Comp Physiol. 2006;290:R313-21.
35. Vary TC, Lang CH. IGF-I activates the eIF4F system in cardiac muscle in vivo. Mol Cell Biochem. 2005;272:209-20.
36. Vary TC, Lynch CH. Meal feeding stimulates phosphorylation of multiple effector proteins regulating protein synthetic processes in rat hearts. J Nutr. 2006;136:2284-90.
37. Hong S-O, Layman DK. Effects of leucine on in vivo protein synthesis and degradation in rat skeletal muscle. J Nutr. 1984;114:1204-12.
38. Buse MG, Atwell R, Mancusi V. Leucine a possible regulator of protein turnover in muscle. J Clin Invest. 1975;56:1250-61.
39. Svenberg E, Moller-Loswick A-C, Mathews DE, Korner U, Anderson M, Lundholm K. Effects of amino acids on synthesis and degradation of skeletal muscle proteins in humans. Am J Physiol Endocrinol Metab. 1996;271:E718-24.
40. Giordano M, Castellino P, DeFronzo RA. Differential responsiveness of protein synthesis and protein degradation to amino acid availability in humans. Diabetes. 1996;45:393-9.
41. Bennet WM, Connacher AA, Scrimgeour CM, Smith K, Rennie MJ. Increase in anterior tibialis muscle protein synthesis in healthy man during mixed amino acid infusion: studies of incorporation of [1-13C]leucine. Clin Sci. 1989;76:447-54.
42. Bennet WM, Connacher AA, Scrimgeour CM, Rennie MJ. The effect of amino acid infusion on leg protein turnover assessed by L-[15N]phenylalanine and L-[1-13C]leucine exchange. Eur J Clin Invest. 1990;20:41-50.
43. Fukagawa NK, Minaker KL, Young VR, Matthews DE, Bier DM, Rowe JW. Leucine metabolism in aging humans: effects of insulin and substrate availability. Am J Physiol Endocrinol Metab. 1989;256:E288-94.
44. Tessari P, Inchiostro S, Biolo G, Trevisan R, Fantin G, Marescotti MC, Iori E, Tiengo A, Crepaldi G. Differential effects hyperinsulinemia and hyper-aminoacidemia on leucine-carbon metabolism in vivo. Role of substrate availability on estimates of whole-body protein synthesis. J Clin Invest. 1987;79:1062-9.
45. Preedy VR, Garlick PJ. The response of muscle protein synthesis to nutrient intake in post-absorptive rats: the role of insulin and amino acids. Biosci Rep. 1986;6:177-83.
46. Svanberg E, Zachrisson H, Ohlsson C, Iresjo B-M, Lindholm KG. Role of insulin and IGF-I in activation of muscle protein synthesis after oral feeding. Am J Physiol Endocrinol Metab. 1996;270:E614-20.
47. Vary TC, Murphy JM. Role of extrasplanchnic organs in the metabolic response to sepsis: effect of insulin. Circ Shock. 1989;29:41-57.
48. Anthony JC, Lang CH, Crozier SJ, Anthony TG, MacLean DA, Kimball SR, Jefferson LS. Contribution of insulin to the translational control of protein synthesis in skeletal muscle by leucine. Am J Physiol Endocrinol Metab. 2002;282:E1092-101.
49. Vary TC, Lynch CJ. Biochemical approaches for nutritional support of skeletal muscle protein metabolism during sepsis. Nutr Res Rev. 2004;17:77-88.
50. Vary TC, Lynch CJ. Nutrient signaling to muscle and adipose tissue by leucine. In: J. Zempleni and K. Dakshinamurti, editors. Nutrients and cell signaling. New York: Marcel Dekkar; 2005. p. 299-327.
51. Chua B, Siehl DL, Morgan HE. Effect of leucine and metabolites of branched chain amino acids on protein turnover in heart. J Biol Chem. 1979;254:8358-62.
52. Chua BH, Siehl DL, Morgan HE. A role for leucine in regulation of protein turnover in working rat hearts. Am J Physiol Endocrinol Metab. 1980;239:E510-4.
53. Chua BHL, Siehl DL, Fuller EO, Morgan HE. Effects of cardiac work and leucine on protein turnover. Adv Myocardiol. 1983;4:115-25.
54. Tischler M, Desautels M, Goldberg A. Does leucine, leucyl-tRNA, or some other metabolite of leucine regulate protein synthesis and degradation in skeletal and cardiac muscle? J Biol Chem. 1982;257:1613-21.
55. May ME, Buse MG. Effects of branched-chain amino acids on protein turnover. Diabetes Metab Rev. 1989;5:227-45.
56. Flaim KE, Copenhaver ME, Jefferson LS. Effects of diabetes on protein synthesis in fast- and slow-twitch rat skeletal muscle. Am J Physiol Endocrinol Metab. 1980;239:E88-95.
57. Xu G, Kwon G, Marshall C, Lin T-A, Lawrence J Jr, McDaniel M. Branched-chain amino acids are essential in the regulation of PHAS-I and p70 S6 kinase by pancreatic b-cells. J Biol Chem. 1998;273:28178-84.
58. Lang CH, Frost RA, Deshpande N, Kumar V, Vary TC, Jefferson LS, Kimball SR. Alcohol impairs leucine-mediated phosphorylation of 4E-BP1, S6K1, eIF4G, and mTOR in skeletal muscle. Am J Physiol Endocrinol Metab. 2003;285:E1205-15.
59. Anthony JC, Yoshizawa F, Anthony TG, Vary TC, Jefferson LS, Kimball SR. Leucine stimulates translation initiation in skeletal muscle of postabsorptive rats via a rapamycin-sensitive pathway. J Nutr. 2000;130:2413-9.
60. Bolster DR, Vary TC, Kimball SR, Jefferson LS. Leucine regulates translation initiation in rat skeletal muscle via enhanced eIF4G phosphorylation. J Nutr. 2004;134:1704-10.
61. Escobar J, Frank JW, Suryawan A, Nguyen HV, Kimball SR, Jefferson LS, Davis TA. Regulation of cardiac and skeletal muscle protein synthesis by individual branched-chain amino acids in neonatal pigs. Am J Physiol Endocrinol Metab. 2006;290:E612-21.
62. Lynch CJ, Fox HE, Vary TC, Jefferson LS, Kimball SR. Regulation of amino-acid sensitive TOR signaling by leucine analogs in adipocytes. J Cell Biochem. 2000;77:234-51.
63. Lynch CJ, Hutson SM, Patson BJ, Vaval A, Vary TC. Tissue-specific effects of chronic dietary leucine and norleucine supplementation on protein synthesis in rats. Am J Physiol Endocrinol Metab. 2002;283:E824-35.
64. Lynch CJ, Halle B, Fujii H, Vary TC, Wallin R, Damuni Z, Hutson SM. Potential role of leucine metabolism in the leucine signaling pathway involving mTOR. Am J Physiol Endocrinol Metab. 2003;285:E854-63.
65. Li JB, Jefferson LS. Influence of amino acid availability on protein turnover in perfused skeletal muscle. Biochim Biophys Acta. 1978;544:351-9.
66. Anthony JC, Anthony TG, Kimball SR, Jefferson LS. Signaling pathway involved in translation control of protein synthesis in skeletal muscle by leucine. J Nutr. 2001;131:S856-60.
67. Loewith R, Jacinto E, Wullschlager S, Lorberg A, Crespo JL, Bonenfant D, Opplinger W, Jenoe P, Hall MN. Two TOR complexes, only one of which is rapamycin sensitive, have distinct roles in cell growth control. Mol Cell. 2002;10:457-68.
68. Hara K, Maruki Y, Long X, Yoshino K, Oshiro N, Hidayat S, Tokuagna C, Avrch J, Yonezawa K. Raptor, binding partner of target of rapamycin (TOR), mediates TOR action. Cell. 2002;110:177-89.
69. Kim D-H, Sarbassov DD, Ali SM, King JE, Latek RR, Erdjumnet-Bromage H, Tempest P, Sabatini DM. mTOR interacts with raptor to form a nutrient-sensitive complex that signals to cell growth machinery. Cell. 2002;110:163-75.
70. Abraham RT. Identification of TOR signaling complexes: more TORC for the cell growth engine. Cell. 2002;111:9-12.
71. Yang Q, Inoki K, Ikenoue T, Guan K-L. Identification of Sin1 as an essential TORC2 component required for complex formation and kinase activity. Genes Dev. 2006;20:2820-32.
72. van Slegtenhorst M, Nellist M, Nagelkerken B, Cheadle J, Snell R, van den Ouweland A, Reuser A, Sampson J, Halley D, et al. Interaction between hamartin and tuberlin, the TSC1 and TSC2 gene products. Hum Mol Genet. 1998;7:1053-7.
73. Tee AR, Fingar DC, Manning BD, Kwiatkowski DJ, Cantley LC, Blenis J. Tuberous sclerosis complex-1 and -2 gene products function together to inhibit mammalian target of rapamycin (mTOR)-mediated downstream signaling. Proc Natl Acad Sci USA. 2002;99:13571-6.
74. Garami A, Zwartkruis FJT, Nobukuni T, Joaquin M, Roccio M, Stocker H, Kozma SC, Hafen E, Bos JL, et al. Insulin activation of Rheb, a mediator of mTOR/S6K/4E-BP signaling, is inhibited by TSC1 and TSC2. Mol Cell. 2003;11:1457-66.
75. Inoki K. Rheb GTPase is a direct target of TSC2 GAP activity and regulates mTOR signaling. Genes Dev. 2003;17:1829-34.
76. Zhang Y, Gao X, Saucedo L, Ru B, Edgar BA, Pan D. Rheb is a direct target of the tuberous sclerosis tumor suppressor proteins. Nat Cell Biol. 2003;5:578-81.
77. Takai Y. Small GTP-binding proteins. Physiol Rev. 2001;81:153-208.
78. Paduch M. Structure of small G proteins and their regulators. Acta Biochim Pol. 2001;48:829-50.
79. Maheshwar MM, Cheadle WJ, Jones AC, Myring J, Fryer AE, Harris PC, Sampson, JR. GAP-related domain of tuberin, the product of TSC2 gene, is a target for missense mutations in tuberous sclerosis. Hum Mol Genet. 1997;6:1991-6.
80. Jaeschke A, Hartkamp J, Saitoh M, Roworth W, Nobukuni T, Hodges A, Sampson J, Thomas G, Lamb R. Tuberous sclerosis complex suppressor mediated S6 kinase inhibition by phosphotidylinositide-3-OH linase is mTOR independent. J Cell Biol. 2002;159:217-24.
81. Potter CJ, Pedrazza LG, Xu T. AKT regulates growth by directly phosphorylating TSC2. Nat Cell Biol. 2002;4:658-62.
82. Roux PP, Ballif BA, Anjun R, Gygi SP, Blenis J. Tumor-promoting phorbol esters and activated Ras inactivate the tuberous sclerosis tumor suppressor complex via p90 ribosomal S6 kinase. Proc Natl Acad Sci USA. 2004;101:13489-94.
83. Ma L, Chen Z, Erdjumeent-Bromage H, Tempst P, Pandoffi PP. Phosphorylation and functional inactivation of TSC2 by Erk: implications for tuberous sclerosis and cancer pathogenesis. Cell. 2005;121:179-93.
84. Li Y, Inoki K, Vacratsis P, Guan K-L. The p38 and MK2 kinase cascade phosphorylates tuberin, the tuberous sclerosis 2 gene product, and enhances its interaction with 14-3-3. J Biol Chem. 2003;278:13663-71.
85. Dan HC, Sun M, Yang L, Feldman RI, Sui X-M, Ou CC, Nellist M, Yeung RS, Halley DJJ, et al. Phosphatidylinositol 3-kinase/AKT pathway regulates tuberous sclerosis tumor suppressor complex by phosphorylation of tuberin. J Biol Chem. 2002;277:35364-70.
86. Aicher LD, Campbell JS, Yeung RS. Tuberlin phosphorylation regulates its interaction with hamartin. J Biol Chem. 2001;276:21017-21.
87. Manning BD, Tee AR, Logsdon MN, Blenis J, Cantley LC. Identification of the tuberous sclerosis complex-2 tumor suppressor gene product tuberlin as a target of the phosphoinositide 3-kinase/ Akt pathway. Mol Cell. 2002;10:151-62.
88. Chung J, Kuo CJ, Crabtree GR, Blenis J. Rapamycin-FKBP specifically blocks growth-dependent activation of and signaling by the 70 kDa S6 protein kinases. Cell. 1992;69:1227-36.
89. Price DJ, Grove JR, Calvo V, Avruch J, Bierer BE. Rapamycin-induced inhibition of the 70-kilodalton S6 protein kinase. Science. 1992;257:973-7.
90. Vary TC, Anthony JC, Jefferson LS, Kimball SR, Lynch CJ. Rapamycin blunts nutrient stimulation of eIF4G, but not PKCe phosphorylation in skeletal. Am J Physiol Endocrinol Metab. 2007 March 27; [Epub ahead of print].
91. Fox HL, Kimball SR, Jefferson LS, Lynch CJ. Amino acids stimulate phosphorylation of p70S6k and organization of rat adipocytes into multicellular clusters. Am J Physiol Cell Physiol. 1998;274:C206-13.
92. Fox HL, Pham PT, Kimball SR, Jefferson LS, Lynch CJ. Amino acid effects on translation repressor 4E-BP1 are mediated primarily by L-leucine in isolated adipocytes. Am J Physiol Cell Physiol. 1998;275:C1232-8.
93. Vary TC, Goodman S, Kilpatrick LE, Lynch CJ. Nutrient regulation of PCKe is mediated by leucine, not insulin, in skeletal muscle. Am J Physiol Endocrinol Metab. 2005;289:E684-94.
94. Dardevet D, Sornet C, Vary TC, Grizard J. Phosphatidylinositol 3-kinase and p70 S6 kinase participate in regulation of protein turnover in skeletal muscle by insulin and IGF-I. Endocrinology. 1996;137:4087-94.
95. Meyuhas O, Hornstein E, Stolovich M, Levy G, Livingstone M, Templeton D, Avruch J, Meyuhas O. Amino acid-induced translation of TOP mRNA is fully dependent on phosphatidyl 3-kinase-mediated signaling is partially inhibited by rapamycin, and is independent of S6K1 and rpS6 phosphorylation. Mol Cell Biol. 2001;21:8671-83.
96. Davis TA, Fioretto ML, Nguygen HV, Reeds PJ. Protein turnover in skeletal muscle of suckling rats. Am J Physiol Reg Integr Comp Physiol. 1989;257:R1141-6.
97. Denne SC, Kalhan SC. Leucine metabolism in human newborns. Am J Physiol Endocrinol Metab. 1987;253:E608-15.
98. O'Connor PM, Kimball SR, Suryawan A, Bush JA, Nguyen HV, Jeferson L, Davis TA. Regulation of translation initiation by insulin and amino acids in skeletal muscle of neonatal pigs. Am J Physiol Endocrinol Metab. 2003;285:E40-53.
99. Escobar J, Frank JW, Suryawan A, Nguyen HV, Kimball SR, Jeferson L, Davis TA. Physiological rise in plasma leucine stimulates muscle protein synthesis in neonatal pigs by enhancing translation initiation factor activation. Am J Physiol Endocrinol Metab. 2005;288:E914-21.
100. Dardevet D, Sornet C, Balage M, Grizard J. Stimulation of in vitro rat muscle protein synthesis by leucine decreases with age. J Nutr. 2000;130:2630-5.
101. Dardevet D, Sornet C, Bayle G, Prugnaud J, Pouyet C, Grizard J. Postprandial stimulation of muscle protein synthesis in old rats can be restored by a leucine-supplemented meal. J Nutr. 2002;132:95-100.
102. Rieu I, Sornet C, Bayle G, Prugnaud J, Pouyet C, Balage M, Papet I, Grizard J, Dardevet D. Leucine-supplemented meal feeding for ten days beneficially affects postprandial muscle protein synthesis in old rats. J Nutr. 2003;133:1198-205.