Mammalian target of rapamycin pathway is up-regulated by both acute endurance exercise and chronic muscle contraction in rat skeletal muscle

Applied Physiology, Nutrition and Metabolism

Volumn 38, Issue 8, 2013, Pages 862-869

  Edgett, Brittany A ^a   Fortner, Melanie L ^a   Bonen, Arend ^b   Gurd, Brendon J ^a  

^a QUEEN S UNIVERSITY   (Canada)

^b UNIVERSITY OF GUELPH   (Canada)

Author keywords

eIF2; Exercise; mTOR; RpS6; S6K1; Training

Indexed keywords

RAPAMYCIN;

ANIMAL; METABOLISM; MUSCLE CONTRACTION; PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; SPRAGUE DAWLEY RAT;

ANIMALS; MUSCLE CONTRACTION; MUSCLE, SKELETAL; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; SIROLIMUS;

EID: 84880318105     PISSN: 17155312     EISSN: 17155320     Source Type: Journal    
DOI: 10.1139/apnm-2012-0405     Document Type: Article

References (50)

1. Armstrong, J.L., Bonavaud, S.M., Toole, B.J., and Yeaman, S.J. 2001. Regulation of glycogen synthesis by amino acids in cultured human muscle cells. J. Biol. Chem. 276(2): 952-956. doi:10.1074/jbc.M004812200. PMID:11013237.
2. Bentzinger, C.F., Romanino, K., Cloëtta, D., Lin, S., Mascarenhas, J.B., Oliveri, F., Xia, J., Casanova, E., Costa, C.F., Brink, M., Zorzato, F., Hall, M.N., and Rüegg, M.A. 2008. Skeletal muscle-specific ablation of raptor, but not of rictor, causes metabolic changes and results in muscle dystrophy. Cell. Metab. 8(5): 411-424. doi:10.1016/j.cmet.2008.10.002. PMID:19046572.
3. Benziane, B., Burton, T.J., Scanlan, B., Galuska, D., Canny, B.J., Chibalin, A.V., Zierath, J.R., and Stepto, N.K. 2008. Divergent cell signaling after short-term intensified endurance training in human skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 295(6): E1427-E1438. doi:10.1152/ajpendo.90428.2008. PMID:18827172.
4. Bolster, D.R., Kubica, N., Crozier, S.J., Williamson, D.L., Farrell, P.A., Kimball, S.R., and Jefferson, L.S. 2003. Immediate response of mammalian target of rapamycin (mTOR)-mediated signalling following acute resistance exerciseinratskeletalmuscle. J.Physiol.553(Pt1):213-220. doi:10.1113/jphysiol. 2003.047019.
5. Camera, D.M., Edge, J., Short, M.J., Hawley, J.A., and Coffey, V.G. 2010. Early time course of Akt phosphorylation after endurance and resistance exercise. Med. Sci. Sports Exerc. 42(10): 1843-1852. doi:10.1249/MSS.0b013e3181d964e4. PMID:20195183.
6. Campbell, S.E., Tandon, N.N., Woldegiorgis, G., Luiken, J.J.F.P., Glatz, J.F.C., and Bonen, A. 2004. A novel function for fatty acid translocase (FAT)/CD36: involvement in long chain fatty acid transfer into the mitochondria. J. Biol. Chem. 279: 36235-36241. doi:10.1074/jbc.M400566200. PMID:15161924.
7. Carter, H.N., and Hood, D.A. 2012. Contractile activity-induced mitochondrial biogenesis and mTORC1. Am. J. Physiol. Cell. Physiol. 303(5): C540-C547. doi:10.1152/ajpcell.00156.2012.
8. Cunningham, J.T., Rodgers, J.T., Arlow, D.H., Vazquez, F., Mootha, V.K., and Puigserver, P. 2007. mTOR controls mitochondrial oxidative function through a YY1-PGC-1α transcriptional complex. Nature, 450(7170): 736-740. doi:10.1038/nature06322. PMID:18046414.
9. D'Antona, G., Ragni, M., Cardile, A., Tedesco, L., Dossena, M., Bruttini, F., Caliaro, F., Corsetti, G., Bottinelli, R., Carruba, M.O., Valerio, A., and Nisoli, E. 2010. Branched-chain amino acid supplementation promotes survival and supports cardiac and skeletal muscle mitochondrial biogenesis in middleaged mice. Cell. Metab. 12(4): 362-372. doi:10.1016/j.cmet.2010.08.016. PMID: 20889128.
10. Deldicque, L., Atherton, P., Patel, R., Theisen, D., Nielens, H., Rennie, M.J., and Francaux, M. 2008a. Decrease in Akt/PKB signalling in human skeletal muscle by resistance exercise. Eur. J. Appl. Physiol. 104(1): 57-65. doi:10.1007/ s00421-008-0786-7. PMID:18535836.
11. Deldicque, L., Atherton, P., Patel, R., Theisen, D., Nielens, H., Rennie, M.J., and Francaux, M. 2008b. Effects of resistance exercise with and without creatine supplementation on gene expression and cell signaling in human skeletal muscle. J. Appl. Physiol. 104(2): 371-378. doi:10.1152/japplphysiol.00873.2007. PMID:18048590.
12. Dreyer, H.C., Drummond, M.J., Pennings, B., Fujita, S., Glynn, E.L., Chinkes, D.L., Dhanani, S., Volpi, E., and Rasmussen, B.B. 2008. 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(2): E392-E400. doi:10.1152/ajpendo.00582. 2007. PMID:18056791.
13. Dupont, E., Cieniewski-Bernard, C., Bastide, B., and Stevens, L. 2011. Electrostimulation during hindlimb unloading modulates PI3K-AKT downstream targets without preventing soleus atrophy and restores slow phenotype through ERK. Am. J. Physiol. Regul. Integr. Comp. Physiol. 300(2): R408-R417. doi:10.1152/ajpregu.00793.2009. PMID:21106911.
14. Farnfield, M.M., Breen, L., Carey, K.A., Garnham, A., and Cameron-Smith, D. 2012. Activation of mTOR signalling in young and old human skeletal muscle in response to combined resistance exercise and whey protein ingestion. Appl. Physiol. Nutr. Metab. 37(1): 21-30. doi:10.1139/h11-132. PMID:22148961.
15. Glynn, E.L., Lujan, H.L., Kramer, V.J., Drummond, M.J., DiCarlo, S.E., and Rasmussen, B.B. 2008. A chronic increase in physical activity inhibits fedstate mTOR/S6K1 signaling and reduces IRS-1 serine phosphorylation in rat skeletal muscle. Appl. Physiol. Nutr. Metab. 33(1): 93-101. doi:10.1139/H07-149. PMID:18347658.
16. Gurd, B.J., Yoshida, Y., Lally, J., Holloway, G.P., and Bonen, A. 2009. The deacetylase enzyme SIRT1 is not associated with oxidative capacity in rat heart and skeletal muscle and its overexpression reduces mitochondrial biogenesis. J. Physiol. 587(Pt 8): 1817-1828. doi:10.1113/jphysiol.2008.168096.
17. Gurd, B.J., Yoshida, Y., McFarlan, J.T., Holloway, G.P., Moyes, C.D., Heigenhauser, G.J., Spriet, L., and Bonen, A. 2011. Nuclear SIRT1 activity, but not protein content, regulates mitochondrial biogenesis in rat and human skeletal muscle. Am. J. Physiol. Regul. Integr. Comp. Physiol. 301(1): R67-R75. doi:10.1152/ajpregu.00417.2010. PMID:21543634.
18. Gurd, B.J., Holloway, G.P., Yoshida, Y., and Bonen, A. 2012. In mammalian muscle, SIRT3 is present in mitochondria and not in the nucleus; and SIRT3 is upregulated by chronic muscle contraction in an adenosine monophosphateactivated protein kinase-independent manner. Metabolism, 61(5): 733-741. doi:10.1016/j.metabol.2011.09.016. PMID:22078938.
19. Gwag, T., Lee, K., Ju, H., Shin, H., Lee, J.W., and Choi, I. 2009. Stress and signaling responses of rat skeletal muscle to brief endurance exercise during hindlimb unloading: a catch-up process for atrophied muscle. Cell. Physiol. Biochem. 24(5-6): 537-546. doi:10.1159/000257510. PMID:19910694.
20. Hara, K., Yonezawa, K., Kozlowski, M.T., Sugimoto, T., Andrabi, K., Weng, Q.P., Kasuga, M., Nishimoto, I., and Avruch, J. 1997. Regulation of eIF-4E BP1 phosphorylation by mTOR. J. Biol. Chem. 272(42): 26457-26463. doi:10.1074/jbc. 272.42.26457. PMID:9334222.
21. Holloszy, J.O. 2008. Regulation by exercise of skeletal muscle content of mitochondria and GLUT4. J. Physiol. Pharmacol. 59(Suppl. 7): 5-18.
22. Holloszy, J.O., and Coyle, E.F. 1984. Adaptations of skeletal muscle to endurance exercise and their metabolic consequences. J. Appl. Physiol. 56(4): 831-838. PMID:6373687.
23. Hood, D.A. 2009. Mechanisms of exercise-induced mitochondrial biogenesis in skeletal muscle. Appl. Physiol. Nutr. Metab. 34(3): 465-472. doi:10.1139/H09-045. PMID:19448716.
24. Hulmi, J.J., Tannerstedt, J., Selänne, H., Kainulainen, H., Kovanen, V., and Mero, A.A. 2009. Resistance exercise with whey protein ingestion affects mTOR signaling pathway and myostatin in men. J. Appl. Physiol. 106(5): 1720-1729. doi:10.1152/japplphysiol.00087.2009. PMID:19299575.
25. Kimball, S.R. 1999. Eukaryotic initiation factor eIF2. Int. J. Biochem. Cell Biol. 31(1): 25-29. doi:10.1016/S1357-2725(98)00128-9. PMID:10216940.
26. Kimball, S.R., and Jefferson, L.S. 2010. Control of translation initiation through integration of signals generated by hormones, nutrients, and exercise. J. Biol. Chem. 285(38): 29027-29032. doi:10.1074/jbc.R110.137208. PMID:20576612.
27. Kubica, N., Kimball, S.R., Jefferson, L.S., and Farrell, P.A. 2004. Alterations in the expression of mRNAs and proteins that code for species relevant to eIF2B activity after an acute bout of resistance exercise. J. Appl. Physiol. 96(2): 679-687. doi:10.1152/japplphysiol.00962.2003. PMID:14565967.
28. Kubica, N., Bolster, D.R., Farrell, P.A., Kimball, S.R., and Jefferson, L.S. 2005. Resistance exercise increases muscle protein synthesis and translation of eukaryotic initiation factor 2B mRNA in a mammalian target of rapamycindependent manner. J. Biol. Chem. 280(9): 7570-7580. doi:10.1074/jbc. M413732200. PMID:15591312.
29. Kumar, A., Lawrence, J.C., Jr., Jung, D.Y., Ko, H.J., Keller, S.R., Kim, J.K., Magnuson, M.A., and Harris, T.E. 2010. Fat cell-specific ablation of rictor in mice impairs insulin-regulated fat cell and whole-body glucose and lipid metabolism. Diabetes, 59(6): 1397-1406. doi:10.2337/db09-1061. PMID: 20332342.
30. Leger, B., Cartoni, R., Praz, M., Lamon, S., Deriaz, O., Crettenand, A., Gobelet, C., Rohmer, P., Konzelmann, M., Luthi, F., and Russell, A.P. 2006. Akt signaling through GSK-3, mTOR and Foxo1 is involved in human skeletal muscle hypertrophy and atrophy. J. Physiol. 576(Pt 3): 923-933. doi:10.1113/jphysiol. 2006.116715.
31. Mader, S., Lee, H., Pause, A., and Sonenberg, N. 1995. The translation initiation factor eIF-4E binds to a common motif shared by the translation factor eIF-4 gamma and the translational repressors 4E-binding proteins. Mol. Cell. Biol. 15(9): 4990-4997. PMID:7651417.
32. Marcotrigiano, J., Gingras, A.C., Sonenberg, N., and Burley, S.K. 1999. Capdependent translation initiation in eukaryotes is regulated by a molecular mimic of eIF4G. Mol. Cell. 3(6): 707-716. doi:10.1016/S1097-2765(01)80003-4. PMID:10394359.
33. Mascher, H., Andersson, H., Nilsson, P.A., Ekblom, B., and Blomstrand, E. 2007. Changes in signalling pathways regulating protein synthesis in human muscle in the recovery period after endurance exercise. Acta Physiol. (Oxf.), 191(1): 67-75. doi:10.1111/j.1748-1716.2007.01712.x.
34. Mayhew, D.L., Kim, J.S., Cross, J.M., Ferrando, A.A., and Bamman, M.M. 2009. Translational signaling responses preceding resistance training-mediated myofiber hypertrophy in young and old humans. J. Appl. Physiol. 107(5): 1655-1662. doi:10.1152/japplphysiol.91234.2008. PMID:19589955.
35. McCullagh, K.J.A., Juel, C., O'Brien, M., and Bonen, A. 1996. Chronic muscle stimulation increases lactate transport in rat skeletal muscle. Mol. Cell. Biochem. 156(1): 51-57. PMID:8709976.
36. Morrison, P.J., Hara, D., Ding, Z., and Ivy, J.L. 2008. Adding protein to a carbohydrate supplement provided after endurance exercise enhances 4E-BP1 and RPS6 signaling in skeletal muscle. J. Appl. Physiol. 104(4): 1029-1036. doi:10. 1152/japplphysiol.01173.2007. PMID:18239077.
37. Murphy, K.T., Petersen, A.C., Goodman, C., Gong, X., Leppik, J.A., Garnham, A.P., Cameron-Smith, D., Snow, R.J., and McKenna, M.J. 2006. Prolonged submaximal exercise induces isoform-specific Na+-K+-ATPase mRNA and protein responses in human skeletal muscle. Am. J. Physiol. Regul. Integr. Comp. Physiol. 290(2): R414-R424. doi:10.1152/ajpregu.00172.2005. PMID:16179492.
38. Pasini, E., Le Douairon Lahaye, S., Flati, V., Assanelli, D., Corsetti, G., Speca, S., Bernabei, R., Calvani, R., and Marzetti, E. 2012. Effects of treadmill exercise and training frequency on anabolic signaling pathways in the skeletal muscle of aged rats. Exp. Gerontol. 47(1): 23-28. doi:10.1016/j.exger.2011.10.003. PMID:22015326.
39. Perry, C.G., Lally, J., Holloway, G.P., Heigenhauser, G.J., Bonen, A., and Spriet, L.L. 2010. Repeated transient mRNA bursts precede increases in transcriptional and mitochondrial proteins during training in human skeletal muscle. J. Physiol. 588(Pt 23): 4795-4810. doi:10.1113/jphysiol.2010.199448.
40. Risson, V., Mazelin, L., Roceri, M., Sanchez, H., Moncollin, V., Corneloup, C., Richard-Bulteau, H., Vignaud, A., Baas, D., Defour, A., Freyssenet, D., Tanti, J.F., Le-Marchand-Brustel, Y., Ferrier, B., Conjard-Duplany, A., Romanino, K., Bauché, S., Hantaï, D., Mueller, M., Kozma, S.C., Thomas, G., Rüegg, M.A., Ferry, A., Pende, M., Bigard, X., Koulmann, N., Schaeffer, L., and Gangloff, Y.G. 2009. Muscle inactivation of mTOR causes metabolic and dystrophin defects leading to severe myopathy. J. Cell Biol. 187(6): 859-874. doi:10.1083/jcb.200903131. PMID:20008564.
41. Romanino, K., Mazelin, L., Albert, V., Conjard-Duplany, A., Lin, S., Bentzinger, C.F., Handschin, C., Puigserver, P., Zorzato, F., Schaeffer, L., Gangloff, Y.-G., and Rüegg, M.A. 2011. Myopathy caused by mammalian target of rapamycin complex 1 (mTORC1) inactivation is not reversed by restoring mitochondrial function. Proc. Natl. Acad. Sci. U.S.A. 108(51): 20808-20813. doi:10.1073/pnas.1111448109. PMID:22143799.
42. Russell, R.C., Fang, C., and Guan, K.-L. 2011. An emerging role for TOR signaling in mammalian tissue and stem cell physiology. Development, 138(16): 3343-3356. doi:10.1242/dev.058230. PMID:21791526.
43. Ruvinsky, I., and Meyuhas, O. 2006. Ribosomal protein S6 phosphorylation: from protein synthesis to cell size. Trends Biochem. Sci. 31(6): 342-348. doi: 10.1016/j.tibs.2006.04.003. PMID:16679021.
44. Sarbassov, D.D., Guertin, D.A., Ali, S.M., and Sabatini, D.M. 2005. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science, 307(5712): 1098-1101. doi:10.1126/science.1106148. PMID:15718470.
45. Schieke, S.M., Phillips, D., McCoy, J.P., Jr., Aponte, A.M., Shen, R.F., Balaban, R.S., and Finkel, T. 2006. The mammalian target of rapamycin (mTOR) pathway regulates mitochondrial oxygen consumption and oxidative capacity. J. Biol. Chem. 281(37): 27643-27652. doi:10.1074/jbc.M603536200. PMID:16847060.
46. Sutherland, C., and Cohen, P. 1994. The α-isoform of glycogen synthase kinase-3 from rabbit skeletal muscle is inactivated by p70 S6 kinase or MAP kinaseactivated protein kinase-1 in vitro. FEBS Lett. 338(1): 37-42. doi:10.1016/0014-5793(94)80112-6. PMID:8307153.
47. Sutherland, C., Leighton, I.A., and Cohen, P. 1993. Inactivation of glycogen synthase kinase-3 beta by phosphorylation: new kinase connections in insulin and growth-factor signalling. Biochem. J. 296(Pt 1): 15-19.
48. Welsh, G.I., Miller, C.M., Loughlin, A.J., Price, N.T., and Proud, C.G. 1998. Regulation of eukaryotic initiation factor eIF2B: glycogen synthase kinase-3 phosphorylates a conserved serine which undergoes dephosphorylation in responsetoinsulin. FEBSLett.421(2):125-130. doi:10.1016/S0014-5793(97)01548-2. PMID:9468292.
49. Wilkinson, S.B., Phillips, S.M., Atherton, P.J., Patel, R., Yarasheski, K.E., Tarnopolsky, M.A., and Rennie, M.J. 2008. Differential effects of resistance and endurance exercise in the fed state on signalling molecule phosphorylation and protein synthesis in human muscle. J. Physiol. 586(Pt 15): 3701-3717. doi:10.1113/jphysiol.2008.153916.
50. Zanchi, N.E., de Siqueira Filho, M.A., Lira, F.S., Rosa, J.C., Yamashita, A.S., de Oliveira Carvalho, C.R., Seelaender, M., and Lancha-Jr, A.H. 2009. Chronic resistance training decreases MuRF-1 and Atrogin-1 gene expression but does not modify Akt, GSK-3â and p70S6K levels in rats. Eur. J. Appl. Physiol. 106(3): 415-423. doi:10.1007/s00421-009-1033-6. PMID:19306017.