The role of skeletal muscle mTOR in the regulation of mechanical load-induced growth

Journal of Physiology

Volumn 589, Issue 22, 2011, Pages 5485-5501

  Goodman, Craig A ^a   Frey, John W ^a   Mabrey, Danielle M ^a   Jacobs, Brittany L ^a   Lincoln, Hannah C ^a   You, Jae Sung ^a   Hornberger, Troy A ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FORKHEAD TRANSCRIPTION FACTOR; FOX01 TRANSCRIPTION FACTOR; FOX03 TRANSCRIPTION FACTOR; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN KINASE B; RAPAMYCIN; RIBOSOME RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DOSE RESPONSE; DRUG EFFICACY; DRUG MECHANISM; GROWTH INHIBITION; GROWTH REGULATION; HYPERPLASIA; MALE; MECHANICAL LOAD INDUCED HYPERTROPHY; MECHANICAL STRESS; MOLECULAR MECHANICS; MOUSE; MUSCLE HYPERTROPHY; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; PROTEINASE INHIBITION; SKELETAL MUSCLE;

ABLATION TECHNIQUES; ANIMALS; HYPERTROPHY; MALE; MICE; MICE, TRANSGENIC; MUSCLE, SKELETAL; MUTATION; RIBOSOMES; SIROLIMUS; TOR SERINE-THREONINE KINASES; WEIGHT-BEARING;

EID: 81255169943     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2011.218255     Document Type: Article

References (56)

1. Alessi DR, James SR, Downes CP, Holmes AB, Gaffney PRJ, Reese CB & Cohen P (1997). Characterization of a 3-phosphoinositide-dependent protein kinase which phosphorylates and activates protein kinase Bα. Curr Biol 7, 261-269.
2. Avila G, Lee EH, Perez CF, Allen PD & Dirksen RT (2003). FKBP12 binding to RyR1 modulates excitation-contraction coupling in mouse skeletal myotubes. J Biol Chem 278, 22 600-22 608.
3. Baar K & Esser K (1999). Phosphorylation of p70(S6k) correlates with increased skeletal muscle mass following resistance exercise. Am J Physiol Cell Physiol 276, C120-C127.
4. Bentzinger CF, Romanino K, Cloëtta D, Lin S, Mascarenhas JB, Oliveri F, Xia J, Casanova E, Costa CF, Brink M, Zorzato F, Hall MN & Rüegg MA (2008). Skeletal muscle-specific ablation of raptor, but not of rictor, causes metabolic changes and results in muscle dystrophy. Cell metabolism 8, 411-424.
5. Bodine SC (2006). mTOR signaling and the molecular adaptation to resistance exercise. Med Sci Sports Exerc 38, 1950-1957.
6. Bodine SC, Stitt TN, Gonzalez M, Kline WO, Stover GL, Bauerlein R, Zlotchenko E, Scrimgeour A, Lawrence JC, Glass DJ & Yancopoulos GD (2001). Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol 3, 1014-1019.
7. Brown EJ, Beal PA, Keith CT, Chen J, Shin TB & Schreiber SL (1995). Control of p70 s6 kinase by kinase activity of FRAP in vivo. Nature 377, 441-446.
8. Cavanaugh AH, Hempel WM, Taylor LJ, Rogalsky V, Todorov G & Rothblum LI (1995). Activity of RNA polymerase I transcription factor UBF blocked by Rb gene product. Nature 374, 177-180.
9. Cunningham JT, Rodgers JT, Arlow DH, Vazquez F, Mootha VK & Puigserver P (2007). mTOR controls mitochondrial oxidative function through a YY1-PGC-1α transcriptional complex. Nature 450, 736-740.
10. Dennis PB, Pullen N, Pearson RB, Kozma SC & Thomas G (1998). Phosphorylation sites in the autoinhibitory domain participate in p70s6k activation loop phosphorylation. J Biol Chem 273, 14845-14852.
11. DiPasquale DM, Cheng M, Billich W, Huang SA, van Rooijen N, Hornberger TA & Koh TJ (2007). Urokinase-type plasminogen activator and macrophages are required for skeletal muscle hypertrophy in mice. Am J Physiol Cell Physiol 293, C1278-1285.
12. Drummond GB (2009). Reporting ethical matters in The Journal of Physiology: standards and advice. J Physiol 587, 713-719.
13. Drummond MJ, Fry CS, Glynn EL, Dreyer HC, Dhanani S, Timmerman KL, Volpi E & Rasmussen BB (2009). Rapamycin administration in humans blocks the contraction-induced increase in skeletal muscle protein synthesis. J Physiol 587, 1535-1546.
14. Düvel K, Yecies JL, Menon S, Raman P, Lipovsky AI, Souza AL, Triantafellow E, Ma Q, Gorski R, Cleaver S, Vander Heiden MG, MacKeigan JP, Finan PM, Clish CB, Murphy LO & Manning BD (2010). Activation of a Metabolic Gene Regulatory Network Downstream of mTOR Complex 1. Mol Cell 39, 171-183.
15. Erbay E & Chen J (2001). The mammalian target of rapamycin regulates C2C12 myogenesis via a kinase-independent mechanism. J Biol Chem 276, 36079-36082.
16. Ge Y, Wu AL, Warnes C, Liu J, Zhang C, Kawasome H, Terada N, Boppart MD, Schoenherr CJ & Chen J (2009). mTOR regulates skeletal muscle regeneration in vivo through kinase-dependent and kinase-independent mechanisms. Am J Physiol Cell Physiol 297, C1434-1444.
17. Goldberg AL, Etlinger JD, Goldspink DF & Jablecki C (1975). Mechanism of work-induced hypertrophy of skeletal muscle. Med Sci Sports 7, 185-198.
18. Gollnick PD, Timson BF, Moore RL & Riedy M (1981). Muscular enlargement and number of fibers in skeletal muscles of rats. J Appl Physiol 50, 936-943.
19. Goodman CA, Mabrey DM, Frey JW, Miu MH, Schmidt EK, Pierre P & Hornberger TA (2011a). Novel insights into the regulation of skeletal muscle protein synthesis as revealed by a new nonradioactive in vivo technique. FASEB J 25, 1028-1039.
20. Goodman CA, Mayhew DL & Hornberger TA (2011b). Recent progress towards understanding the molecular mechanisms that regulate skeletal muscle mass. Cell Signal (in press).
21. Goodman CA, Miu MH, Frey JW, Mabrey DM, Lincoln HC, Ge Y, Chen J & Hornberger TA (2010). A phosphatidylinositol 3-kinase/protein kinase B-independent activation of mammalian target of rapamycin signaling is sufficient to induce skeletal muscle hypertrophy. Mol Biol Cell 21, 3258-3268.
22. Gottlob K, Majewski N, Kennedy S, Kandel E, Robey RB & Hay N (2001). Inhibition of early apoptotic events by Akt/PKB is dependent on the first committed step of glycolysis and mitochondrial hexokinase. Genes Dev 15, 1406-1418.
23. Hahn-Windgassen A, Nogueira V, Chen C-C, Skeen JE, Sonenberg N & Hay N (2005). Akt activates the mammalian target of rapamycin by regulating cellular ATP level and AMPK activity. J Biol Chem 280, 32081-32089.
24. Hannan RD, Jenkins A, Jenkins AK & Brandenburger Y (2003). Cardiac hypertrophy: a matter of translation. Clin Exp Pharmacol Physiol 30, 517-527.
25. Hornberger TA, Hunter RB, Kandarian SC & Esser KA (2001). Regulation of translation factors during hindlimb unloading and denervation of skeletal muscle in rats. Am J Physiol Cell Physiol 281, C179-C187.
26. Hornberger TA, Stuppard R, Conley KE, Fedele MJ, Fiorotto ML, Chin ER & Esser KA (2004). Mechanical stimuli regulate rapamycin-sensitive signalling by a phosphoinositide 3-kinase-, protein kinase B- and growth factor-independent mechanism. Biochem J 380, 795-804.
27. Hornberger TA, Sukhija KB, Wang XR & Chien S (2007). mTOR is the rapamycin-sensitive kinase that confers mechanically induced phosphorylation of the hydrophobic motif site Thr(389) in p70(S6k). FEBS Lett 581, 4562-4566.
28. Howlett KF, Sakamoto K, Garnham A, Cameron-Smith D & Hargreaves M (2007). Resistance exercise and insulin regulate AS160 and interaction with 14-3-3 in human skeletal muscle. Diabetes 56, 1608-1614.
29. Hurley BF, Hanson ED & Sheaff AK (2011). Strength training as a countermeasure to aging muscle and chronic disease. Sport Med 41, 289-306.
30. Kirwan JP, Hickner RC, Yarasheski KE, Kohrt WM, Wiethop BV & Holloszy JO (1992). Eccentric exercise induces transient insulin resistance in healthy individuals. J Appl Physiol 72, 2197-2202.
31. LeBrasseur NK, Walsh K & Arany Z (2011). Metabolic benefits of resistance training and fast glycolytic skeletal muscle. Am J Physiol Endocrinol Metab 300, E3-E10.
32. Lorenz MC & Heitman J (1995). TOR mutations confer rapamycin resistance by preventing interaction with FKBP12-rapamycin. J Biol Chem 270, 27531-27537.
33. Machida M, Takeda K, Yokono H, Ikemune S, Taniguchi Y, Kiyosawa H & Takemasa T (2011). Reduction of ribosome biogenesis with activation of the mTOR pathway in denervated atrophic muscle. J Cell Physiol (in press, doi:).
34. Maxwell LC, Faulkner JA & Hyatt GJ (1974). Estimation of number of fibers in guinea pig skeletal muscles. J Appl Physiol 37, 259-264.
35. Mayer C & Grummt I (2006). Ribosome biogenesis and cell growth: mTOR coordinates transcription by all three classes of nuclear RNA polymerases. Oncogene 25, 6384-6391.
36. Miyazaki M, McCarthy JJ, Fedele MJ & Esser KA (2011). Early activation of mTORC1 signalling in response to mechanical overload is independent of phosphoinositide 3-kinase/Akt signalling. J Physiol 589, 1831-1846.
37. Nader GA (2007). Muscle growth learns new tricks from an old dog. Nat Med 13, 1016-1018.
38. Nader GA, McLoughlin TJ & Esser KA (2005). mTOR function in skeletal muscle hypertrophy: increased ribosomal RNA via cell cycle regulators. Am J Physiol Cell Physiol 289, C1457-1465.
39. Oshiro N, Yoshino K, Hidayat S, Tokunaga C, Hara K, Eguchi S, Avruch J & Yonezawa K (2004). Dissociation of raptor from mTOR is a mechanism of rapamycin-induced inhibition of mTOR function. Genes Cells 9, 359-366.
40. Osman B, Doller A, Akool el-S, Holdener M, Hintermann E, Pfeilschifter J & Eberhardt W (2009). Rapamycin induces the TGFβ1/Smad signaling cascade in renal mesangial cells upstream of mTOR. Cell Signal 21, 1806-1817.
41. Pedersen BK & Febbraio MA (2008). Muscle as an endocrine organ: focus on muscle-derived interleukin-6. Physiol Rev 88, 1379-1406.
42. Peterson RT, Beal PA, Comb MJ & Schreiber SL (2000). FKBP12-rapamycin-associated protein (FRAP) autophosphorylates at serine 2481 under translationally repressive conditions. J Biol Chem 275, 7416-7423.
43. 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, Bauche S, Hantai D, Mueller M, Kozma SC, Thomas G, Ruegg MA, Ferry A, Pende M, Bigard X, Koulmann N, Schaeffer L & Gangloff Y-G (2009). Muscle inactivation of mTOR causes metabolic and dystrophin defects leading to severe myopathy. J Cell Biol 187, 859-874.
44. 3K/Akt/GSK3 pathways. Nat Cell Biol 3, 1009-1013.
45. Sandri M (2008). Signaling in muscle atrophy and hypertrophy. Physiology 23, 160-170.
46. Saunders RN, Metcalfe MS & Nicholson ML (2001). Rapamycin in transplantation: a review of the evidence. Kidney Int 59, 3-16.
47. Srikanthan P & Karlamangla AS (2011). Relative muscle mass is inversely associated with insulin resistance and prediabetes. findings from the third national health and nutrition examination survey. J Clin Endocrinol Metab 96, 2898-2903.
48. Steinberg GR & Kemp BE (2009). AMPK in health and disease. Physiol Rev 89, 1025-1078.
49. Stitt TN, Drujan D, Clarke BA, Panaro F, Timofeyva Y, Kline WO, Gonzalez M, Yancopoulos GD & Glass DJ (2004). The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol Cell 14, 395-403.
50. Tamaki T, Akatsuka A, Tokunaga M, Uchiyama S & Shiraishi T (1996). Characteristics of compensatory hypertrophied muscle in the rat: I. Electron microscopic and immunohistochemical studies. Anat Rec 246, 325-334.
51. Tzatsos A & Kandror KV (2006). Nutrients suppress phosphatidylinositol 3-kinase/Akt signaling via raptor-dependent mTOR-mediated insulin receptor substrate 1 phosphorylation. Mol Cell Biol 26, 63-76.
52. Um SH, D'Alessio D & Thomas G (2006). Nutrient overload, insulin resistance, and ribosomal protein S6 kinase 1, S6K1. Cell Metab 3, 393-402.
53. Vaughan HS & Goldspink G (1979). Fibre number and fibre size in a surgically overloaded muscle. J Anat 129, 293-303.
54. Wang T & Donahoe PK (2004). The immunophilin FKBP12: a molecular guardian of the TGF-β family type I receptors. Front Biosci 9, 619-631.
55. Young VR (1970). The role of skeletal and cardiac muscle in the regulation of protein metabolism. In Mammalian Protein Metabolism, ed. Munro HN, pp. 585-674. Academic Press, New York.
56. Zoncu R, Efeyan A & Sabatini DM (2011). mTOR: from growth signal integration to cancer, diabetes and ageing. Nat Rev Mol Cell Biol 12, 21-35.