Reduced REDD1 expression contributes to activation of mTORC1 following electrically induced muscle contraction

American Journal of Physiology - Endocrinology and Metabolism

Volumn 307, Issue 8, 2014, Pages E703-E711

  Gordon, Bradley S ^a   Steiner, Jennifer L ^a   Lang, Charles H ^a   Jefferson, Leonard S ^a   Kimball, Scot R ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

Hypertrophy; Overload; Protein synthesis; Resistance exercise; Skeletal muscle

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; REGULATED IN DNA DAMAGE AND DEVELOPMENT 1 PROTEIN; REPRESSOR PROTEIN; UNCLASSIFIED DRUG; DDIT4 PROTEIN, MOUSE; MECHANISTIC TARGET OF RAPAMYCIN COMPLEX 1; MULTIPROTEIN COMPLEX; MUSCLE PROTEIN; RIBOSOMAL PROTEIN S6 KINASE, 70KD, POLYPEPTIDE 1; S6 KINASE; TARGET OF RAPAMYCIN KINASE; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ECCENTRIC MUSCLE CONTRACTION; ELECTROSTIMULATION; MALE; MOUSE; MUSCLE CONTRACTION; NONHUMAN; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; SCIATIC NERVE; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; TIBIALIS ANTERIOR MUSCLE; 129 MOUSE; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; DOWN REGULATION; ENZYME ACTIVATION; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; HINDLIMB; KNOCKOUT MOUSE; METABOLISM; PHOSPHORYLATION; PROTEIN PROCESSING; UPREGULATION;

ANIMALS; DOWN-REGULATION; ELECTRIC STIMULATION; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; HINDLIMB; MALE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MULTIPROTEIN COMPLEXES; MUSCLE CONTRACTION; MUSCLE PROTEINS; MUSCLE, SKELETAL; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RIBOSOMAL PROTEIN S6 KINASES, 70-KDA; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; TRANSCRIPTION FACTORS; UP-REGULATION;

EID: 84908052263     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00250.2014     Document Type: Article

References (52)

1. 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 130: 2413-2419, 2000.
2. S6k correlates with increased skeletal muscle mass following resistance exercise. Am J Physiol Cell Physiol 276: C120-C127, 1999.
3. Baehr LM, Tunzi M, Bodine SC. Muscle hypertrophy is associated with increases in proteasome activity that is independent of MuRF1 and MAFbx expression. Front Physiol 5: 69, 2014.
4. Bodine SC, Stitt TN, Gonzalez M, Kline WO, Stover GL, Bauerlein R, Zlotchenko E, Scrimgeour A, Lawrence JC, Glass DJ, Yancopoulos GD. Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol 3: 1014-1019, 2001.
5. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254, 1976.
6. Brafman A, Mett I, Shafir M, Gottlieb H, Damari G, Gozlan-Kelner S, Vishnevskia-Dai V, Skaliter R, Einat P, Faerman A, Feinstein E, Shoshani T. Inhibition of oxygen-induced retinopathy in RTP801-deficient mice. Invest Ophthalmol Vis Sci 45: 3796-3805, 2004.
7. Castro AF, Rebhun JF, Clark GJ, Quilliam LA. Rheb binds tuberous sclerosis complex 2 (TSC2) and promotes S6 kinase activation in a rapamycin-and farnesylation-dependent manner. J Biol Chem 278: 32493-32496, 2003.
8. Charbonneau DE, Hanson ED, Ludlow AT, Delmonico MJ, Hurley BF, Roth SM. ACE genotype and the muscle hypertrophic and strength responses to strength training. Med Sci Sports Exerc 40: 677-683, 2008.
9. 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 280: 9769-9772, 2005.
10. Crozier SJ, Kimball SR, Emmert SW, Anthony JC, Jefferson LS. Oral leucine administration stimulates protein synthesis in rat skeletal muscle. J Nutr 135: 376-382, 2005.
11. D'Hulst G, Jamart C, Van Thienen R, Hespel P, Francaux M, Deldicque L. Effect of acute environmental hypoxia on protein metabolism in human skeletal muscle. Acta Physiologica 208: 251-264, 2013.
12. Delgado-Diaz DC, Gordon BS, Dompier T, Burgess S, Dumke C, Mazoue C, Caldwell T, Kostek MC. Therapeutic ultrasound affects IGF-1 splice variant expression in human skeletal muscle. Am J Sports Med 39: 2233-2241, 2011.
13. Dennis MD, Baum JI, Kimball SR, Jefferson LS. Mechanisms involved in the coordinate regulation of mTORC1 by insulin and amino acids. J Biol Chem 286: 8287-8296, 2011.
14. Dennis MD, Jefferson LS, Kimball SR. Role of p70 S6K1-mediated phosphorylation of eIF4B and PDCD4 proteins in the regulation of protein synthesis. J Biol Chem 287: 42890-42899, 2012.
15. Dennis MD, Kimball SR, Jefferson LS. Mechanistic target of rapamycin complex 1 (mTORC1)-mediated phosphorylation is governed by competition between substrates for interaction with raptor. J Biol Chem 288: 10-19, 2013.
16. Dennis MD, McGhee NK, Jefferson LS, Kimball SR. Regulated in DNA damage and development 1 (REDD1) promotes cell survival during serum deprivation by sustaining repression of signaling through the mechanistic target of rapamycin in complex 1 (mTORC1). Cell Signal 25: 2709-2716, 2013.
17. 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, p. ra68.
18. 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 141: 856-862, 2011.
19. 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 294: E392-E400, 2008.
20. Drummond MJ, Fry CS, Glynn EL, Dreyer HC, Dhanani S, Timmerman KL, Volpi E, Rasmussen BB. Rapamycin administration in humans blocks the contraction-induced increase in skeletal muscle protein synthesis. J Physiol 587: 1535-1546, 2009.
21. 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 40: 691-698, 2008.
22. Fry CS, Drummond MJ, Glynn EL, Dickinson JM, Gundermann DM, Timmerman KL, Walker DK, Dhanani S, Volpi E, Rasmussen BB. Aging impairs contraction-induced human skeletal muscle mTORC1 signaling and protein synthesis. Skeletal Muscle 1: 11, 2011.
23. Goodman CA, Frey JW, Mabrey DM, Jacobs BL, Lincoln HC, You JS, Hornberger TA. The role of skeletal muscle mTOR in the regulation of mechanical load-induced growth. J Physiol 589: 5485-5501, 2011.
24. 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 26: 461-467, 2014.
25. Gordon BS, Kelleher AR, Kimball SR. Regulation of muscle protein synthesis and the effects of catabolic states. Int J Biochem Cell Biol 45: 2147-2157, 2013.
26. Hwee DT, Baehr LM, Philp A, Baar K, Bodine SC. Maintenance of muscle mass and load-induced growth in Muscle RING Finger 1-null mice with age. Aging Cell 13: 92-101, 2014.
27. Hwee DT, Bodine SC. Age-related deficit in load-induced skeletal muscle growth. J Gerontol A Biol Sci Med Sci 64: 618-628, 2009.
28. Inoki K, Li Y, Xu T, Guan KL. Rheb GTPase is a direct target of TSC2 GAP activity and regulates mTOR signaling. Genes Dev 17: 1829-1834, 2003.
29. S6k phosphorylation in human skeletal muscle after resistance exercise. Am J Physiol Endocrinol Metab 287: E1-E7, 2004.
30. Katiyar S, Liu E, Knutzen CA, Lang ES, Lombardo CR, Sankar S, Toth JI, Petroski MD, Ronai Z, Chiang GG. REDD1, an inhibitor of mTOR signalling, is regulated by the CUL4A-DDB1 ubiquitin ligase. EMBO Reports 10: 866-872, 2009.
31. Kelleher AR, Kimball SR, Dennis MD, Schilder RJ, Jefferson LS. The mTORC1 signaling repressors REDD1/2 are rapidly induced and activation of p70 S6K1 by leucine is defective in skeletal muscle of an immobilized rat hindlimb. Am J Physiol Endocrinol Metab 304: E229-E236, 2013.
32. Kimball SR, Do AN, Kutzler L, Cavener DR, Jefferson LS. Rapid turnover of the mTOR complex 1 (mTORC1) repressor REDD1 and activation of mTORC1 signaling following inhibition of protein synthesis. J Biol Chem 283: 3465-3475, 2008.
33. Kimball SR, Jefferson LS. Induction of REDD1 gene expression in the liver in response to endoplasmic reticulum stress is mediated through a PERK, eIF2alpha phosphorylation, ATF4-dependent cascade. Biochem Biophys Res Commun 427: 485-489, 2012.
34. 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 279: E1080-E1087, 2000.
35. 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 288: E645-E653, 2005.
36. Kubica N, Bolster DR, Farrell PA, Kimball SR, Jefferson LS. Resistance exercise increases muscle protein synthesis and translation of eukaryotic initiation factor 2Bepsilon mRNA in a mammalian target of rapamycin-dependent manner. J Biol Chem 280: 7570-7580, 2005.
37. Kumar V, Atherton P, Smith K, Rennie MJ. Human muscle protein synthesis and breakdown during and after exercise. J Appl Physiol (1985) 106: 2026-2039, 2009.
38. Liu D, Sartor MA, Nader GA, Gutmann L, Treutelaar MK, Pistilli EE, Iglayreger HB, Burant CF, Hoffman EP, Gordon PM. Skeletal muscle gene expression in response to resistance exercise: sex specific regulation. BMC Genomics 11: 659, 2010.
39. Mayer C, Grummt I. Ribosome biogenesis and cell growth: mTOR coordinates transcription by all three classes of nuclear RNA polymerases. Oncogene 25: 6384-6391, 2006.
40. 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 139: 828-834, 2009.
41. 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 296: C583-C592, 2009.
42. Molitoris JK, McColl KS, Swerdlow S, Matsuyama M, Lam M, Finkel TH, Matsuyama S, Distelhorst CW. Glucocorticoid elevation of dexamethasone-induced gene 2 (Dig2/RTP801/REDD1) protein mediates autophagy in lymphocytes. J Biol Chem 286: 30181-30189, 2011.
43. Murton AJ, Constantin D, Greenhaff PL. The involvement of the ubiquitin proteasome system in human skeletal muscle remodelling and atrophy. Biochim Biophys Acta 1782: 730-743, 2008.
44. O'Neil TK, Duffy LR, Frey JW, Hornberger TA. The role of phosphoinositide 3-kinase and phosphatidic acid in the regulation of mammalian target of rapamycin following eccentric contractions. J Physiol 587: 3691-3701, 2009.
45. Ordway GA, Neufer PD, Chin ER, DeMartino GN. Chronic contractile activity upregulates the proteasome system in rabbit skeletal muscle. J Appl Physiol (1985) 88: 1134-1141, 2000.
46. Phillips SM, Glover EI, Rennie MJ. Alterations of protein turnover underlying disuse atrophy in human skeletal muscle. J Appl Physiol (1985) 107: 645-654, 2009.
47. Sofer A, Lei K, Johannessen CM, Ellisen LW. Regulation of mTOR and cell growth in response to energy stress by REDD1. Mol Cell Biol 25: 5834-5845, 2005.
48. Thomson DM, Brown JD, Fillmore N, Ellsworth SK, Jacobs DL, Winder WW, Fick CA, Gordon SE. AMP-activated protein kinase response to contractions and treatment with the AMPK activator AICAR in young adult and old skeletal muscle. J Physiol 587: 2077-2086, 2009.
49. Vary TC, Anthony JC, Jefferson LS, Kimball SR, Lynch CJ. Rapamycin blunts nutrient stimulation of eIF4G, but not PKCε phosphorylation, in skeletal muscle. Am J Physiol Endocrinol Metab 293: E188-E196, 2007.
50. Vary TC, Lang CH. Assessing effects of alcohol consumption on protein synthesis in striated muscles. Methods Mol Biol 447: 343-355, 2008.
51. 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 117: 246-256, 2014.
52. Witkowski S, Lovering RM, Spangenburg EE. High-frequency electrically stimulated skeletal muscle contractions increase p70s6k phosphorylation independent of known IGF-I sensitive signaling pathways. FEBS Lett 584: 2891-2895, 2010.