Nutrient-induced stimulation of protein synthesis in mouse skeletal muscle is limited by the mTORC1 repressor REDD1

Journal of Nutrition

Volumn 145, Issue 4, 2015, Pages 708-713

  Gordon, Bradley S ^a   Williamson, David L ^b   Lang, Charles H ^a   Jefferson, Leonard S ^a   Kimball, Scot R ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

Author keywords

70 kDa ribosomal protein S6 kinase; Atrophy; DDIT4; Eukaryotic initiation factor 4E binding protein 1; Hypertrophy; Mammalian target of rapamycin; Refeeding

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; PROTEIN; REGULATED IN DEVELOPMENT AND DNA DAMAGE 1; UNCLASSIFIED DRUG; CARRIER PROTEIN; DDIT4 PROTEIN, MOUSE; EIF4EBP1 PROTEIN, MOUSE; MECHANISTIC TARGET OF RAPAMYCIN COMPLEX 1; MULTIPROTEIN COMPLEX; MUSCLE PROTEIN; PHOSPHOPROTEIN; TARGET OF RAPAMYCIN KINASE; TRACE ELEMENT; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; GENE DISRUPTION; GENOTYPE; MALE; MOUSE; NONHUMAN; NUTRIENT; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; REFEEDING; REPRESSOR GENE; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; WESTERN BLOTTING; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; KNOCKOUT MOUSE; METABOLISM; PHOSPHORYLATION;

EUKARYOTA; MAMMALIA; MUS;

ANIMALS; CARRIER PROTEINS; GENE EXPRESSION REGULATION; MALE; MICE; MICE, KNOCKOUT; MICRONUTRIENTS; MULTIPROTEIN COMPLEXES; MUSCLE PROTEINS; MUSCLE, SKELETAL; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN BIOSYNTHESIS; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; TRANSCRIPTION FACTORS;

EID: 84928537903     PISSN: 00223166     EISSN: 15416100     Source Type: Journal    
DOI: 10.3945/jn.114.207621     Document Type: Article

References (38)

1. Phillips SM, Glover EI, Rennie MJ. Alterations of protein turnover underlying disuse atrophy in human skeletal muscle. J Appl Physiol 2009;107:645-54.
2. Crozier SJ, Kimball SR, Emmert SW, Anthony JC, Jefferson LS. Oral leucine administration stimulates protein synthesis in rat skeletal muscle. J Nutr 2005;135:376-82.
3. Dickinson JM, Fry CS, Drummond MJ, Gundermann DM, Walker DK, Glynn EL, Timmerman KL, Dhanani S, Volpi E, Rasmussen BB. Mammalian target of rapamycin complex 1 activation is required for the stimulation of human skeletal muscle protein synthesis by essential amino acids. J Nutr 2011;141:856-62.
4. Dreyer HC, Drummond MJ, Pennings B, Fujita S, Glynn EL, Chinkes DL, Dhanani S, Volpi E, Rasmussen BB. Leucine-enriched essential amino acid and carbohydrate ingestion following resistance exercise enhances mTOR signaling and protein synthesis in human muscle. Am J Physiol Endocrinol Metab 2008;294:E392-400.
5. Gordon BS, Kelleher AR, Kimball SR. Regulation of muscle protein synthesis and the effects of catabolic states. Int J Biochem Cell Biol 2013;45:2147-57.
6. Karlsson HK, Nilsson PA, Nilsson J, Chibalin AV, Zierath JR, Blomstrand E. Branched-chain amino acids increase p70S6k phosphorylation in human skeletal muscle after resistance exercise. Am J Physiol Endocrinol Metab 2004;287:E1-7.
7. Kimball SR, Jefferson LS, Nguyen HV, Suryawan A, Bush JA, Davis TA. Feeding stimulates protein synthesis in muscle and liver of neonatal pigs through an mTOR-dependent process. Am J Physiol Endocrinol Metab 2000;279:E1080-7.
8. Koopman R, Wagenmakers AJ, Manders RJ, Zorenc AH, Senden JM, Gorselink M, Keizer HA, van Loon LJ. Combined ingestion of protein and free leucine with carbohydrate increases postexercise muscle protein synthesis in vivo in male subjects. Am J Physiol Endocrinol Metab 2005;288:E645-53.
9. Cuthbertson D, Smith K, Babraj J, Leese G, Waddell T, Atherton P, Wackerhage H, Taylor PM, Rennie MJ. Anabolic signaling deficits underlie amino acid resistance of wasting, aging muscle. FASEB J 2005;19:422-4.
10. Glover EI, Phillips SM, Oates BR, Tang JE, Tarnopolsky MA, Selby A, Smith K, Rennie MJ. Immobilization induces anabolic resistance in human myofibrillar protein synthesis with low and high dose amino acid infusion. J Physiol 2008;586:6049-61.
11. Kelleher AR, Kimball SR, Dennis MD, Schilder RJ, Jefferson LS. The mTORC1 signaling repressors REDD1/2 are rapidly induced and activation of p70S6K1 by leucine is defective in skeletal muscle of an immobilized rat hindlimb. Am J Physiol Endocrinol Metab 2013;304:E229-36.
12. Kazi AA, Pruznak AM, Frost RA, Lang CH. Sepsis-induced alterations in protein-protein interactions within mTOR complex 1 and the modulating effect of leucine on muscle protein synthesis. Shock 2011;35:117-25.
13. Steiner JL, Lang CH. Alcohol impairs skeletal muscle protein synthesis and mTOR signaling in a time-dependent manner following electrically stimulated muscle contraction. J Appl Physiol 2014;117:1170-9.
14. Thoreen CC, Chantranupong L, Keys HR, Wang T, Gray NS, Sabatini DM. A unifying model for mTORC1-mediated regulation of mRNA translation. Nature 2012;485:109-13.
15. Dennis MD, Baum JI, Kimball SR, Jefferson LS. Mechanisms involved in the coordinate regulation of mTORC1 by insulin and amino acids. J Biol Chem 2011;286:8287-96.
16. Gordon BS, Steiner JL, Lang CH, Jefferson LS, Kimball SR. Reduced REDD1 expression contributes to activation of mTORC1 following electrically induced muscle contraction. Am J Physiol Endocrinol Metab 2014;307:E703-11.
17. McGhee NK, Jefferson LS, Kimball SR. Elevated corticosterone associated with food deprivation upregulates expression in rat skeletal muscle of the mTORC1 repressor, REDD1. J Nutr 2009;139:828-34.
18. Lang CH, Frost RA, Vary TC. Acute alcohol intoxication increases REDD1 in skeletal muscle. Alcohol Clin Exp Res 2008;32:796-805.
19. Puppa MJ, Gao S, Narsale AA, Carson JA. Skeletal muscle glycoprotein 130's role in Lewis lung carcinoma-induced cachexia. FASEB J 2014;28:998-1009.
20. White JP, Gao S, Puppa MJ, Sato S, Welle SL, Carson JA. Testosterone regulation of Akt/mTORC1/FoxO3a signaling in skeletal muscle. Mol Cell Endocrinol 2013;365:174-86.
21. Gordon BS, Kazi AA, Coleman CS, Dennis MD, Chau V, Jefferson LS, Kimball SR. RhoA modulates signaling through the mechanistic target of rapamycin complex 1 (mTORC1) in mammalian cells. Cell Signal 2014;26:461-7.
22. Williamson DL, Li Z, Tuder RM, Feinstein E, Kimball SR, Dungan CM. Altered nutrient response of mTORC1 as a result of changes in REDD1 expression: effect of obesity versus REDD1 deficiency. J Appl Physiol 2014;117:246-56.
23. Drummond MJ, Fujita S, Abe T, Dreyer HC, Volpi E, Rasmussen BB. Human muscle gene expression following resistance exercise and blood flow restriction. Med Sci Sports Exerc 2008;40:691-8.
24. Murakami T, Hasegawa K, Yoshinaga M. Rapid induction of REDD1 expression by endurance exercise in rat skeletal muscle. Biochem Biophys Res Commun 2011;405:615-9.
25. Williamson DL, Kubica N, Kimball SR, Jefferson LS. Exercise-induced alterations in extracellular signal-regulated kinase 1/2 and mammalian target of rapamycin (mTOR) signalling to regulatory mechanisms of mRNA translation in mouse muscle. J Physiol 2006;573:497-510.
26. 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.
27. 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.
28. Yoshizawa F, Kimball SR, Vary TC, Jefferson LS. Effect of dietary protein on translation initiation in rat skeletal muscle and liver. Am J Physiol 1998;275:E814-20.
29. Davis TA. The Avanelle Kirksey Lecture PU. Insulin and amino acids are critical regulators of neonatal muscle growth. Nutr Today 2008;43:143-9.
30. Escobar J, Frank JW, Suryawan A, Nguyen HV, Van Horn CG, Hutson SM, Davis TA. Leucine and alpha-ketoisocaproic acid, but not norleucine, stimulate skeletal muscle protein synthesis in neonatal pigs. J Nutr 2010;140:1418-24.
31. Suryawan A, Davis TA. The abundance and activation of mTORC1 regulators in skeletal muscle of neonatal pigs are modulated by insulin, amino acids, and age. J Appl Physiol (1985) 2010; 109:1448-54.
32. Dennis MD, Coleman CS, Berg A, Jefferson LS, Kimball SR. REDD1 enhances protein phosphatase 2A-mediated dephosphorylation of Akt to repress mTORC1 signaling. Sci Signal 2014;7:ra68.
33. Corradetti MN, Inoki K, Guan KL. The stress-inducted proteins RTP801 and RTP801L are negative regulators of the mammalian target of rapamycin pathway. J Biol Chem 2005;280:9769-72.
34. Wang H, Kubica N, Ellisen LW, Jefferson LS, Kimball SR. Dexamethasone represses signaling through the mammalian target of rapamycin in muscle cells by enhancing expression of REDD1. J Biol Chem 2006;281:39128-34.
35. Miyazaki M, Esser KA. REDD2 is enriched in skeletal muscle and inhibits mTOR signaling in response to leucine and stretch. Am J Physiol Cell Physiol 2009;296:C583-92.
36. Hannan KM, Brandenburger Y, Jenkins A, Sharkey K, Cavanaugh A, Rothblum L, Moss T, Poortinga G, McArthur GA, Pearson RB, et al. mTOR-dependent regulation of ribosomal gene transcription requires S6K1 and is mediated by phosphorylation of the carboxy-terminal activation domain of the nucleolar transcription factor UBF. Mol Cell Biol 2003;23:8862-77.
37. Chang YY, Juhasz G, Goraksha-Hicks P, Arsham AM, Mallin DR, Muller LK, Neufeld TP. Nutrient-dependent regulation of autophagy through the target of rapamycin pathway. Biochem Soc Trans 2009;37:232-6.
38. Braun TP, Grossberg AJ, Krasnow SM, Levasseur PR, Szumowski M, Zhu XX, Maxson JE, Knoll JG, Barnes AP, Marks DL. Cancer-and endotoxin-induced cachexia require intact glucocorticoid signaling in skeletal muscle. FASEB J 2013;27:3572-82.