Mechanotransduction and the regulation of mTORC1 signaling in skeletal muscle

International Journal of Biochemistry and Cell Biology

Volumn 43, Issue 9, 2011, Pages 1267-1276

  Hornberger, Troy A ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Contraction; Exercise; Hypertrophy; Phosphatidic acid and phospholipase D

Indexed keywords

7 METHYLGUANOSINE; AMINO ACID; CALMODULIN; DIACYLGLYCEROL; DIACYLGLYCEROL KINASE; GUANOSINE TRIPHOSPHATASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; LYSOPHOSPHATIDIC ACID; MAMMALIAN TARGET OF RAPAMYCIN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 2; MESSENGER RNA; OLIGONUCLEOTIDE; PHOSPHATIDIC ACID; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOINOSITIDE DEPENDENT PROTEIN KINASE 1; PHOSPHOLIPASE C; PHOSPHOLIPASE D; PROTEIN KINASE B; PROTEIN P70; PUROMYCIN; RAS PROTEIN; RHEB PROTEIN; S6 KINASE; SMALL INTERFERING RNA; SOMATOMEDIN C; TRANSCRIPTION FACTOR FOXO; TUBERIN; UNINDEXED DRUG; WORTMANNIN;

ARTICLE; ENZYME ACTIVITY; GENE MUTATION; HYPERTROPHY; MECHANICAL STIMULATION; MECHANOTRANSDUCTION; MUSCLE MASS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN SYNTHESIS; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SKELETAL MUSCLE;

MAMMALIA;

EID: 79960925868     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2011.05.007     Document Type: Review

References (121)

1. G.R. Adams, and F. Haddad The relationships among IGF-1, DNA content, and protein accumulation during skeletal muscle hypertrophy J Appl Physiol 81 1996 2509 2516 (Pubitemid 27043365)
2. G.R. Adams, and S.A. McCue Localized infusion of IGF-I results in skeletal muscle hypertrophy in rats J Appl Physiol 84 1998 1716 1722 (Pubitemid 28225913)
3. J. Aoki, A. Inoue, K. Makide, N. Saiki, and H. Arai Structure and function of extracellular phospholipase A1 belonging to the pancreatic lipase gene family Biochimie 89 2007 197 204 (Pubitemid 46161954)
4. J.L. Armstrong, S.M. Bonavaud, B.J. Toole, and S.J. Yeaman Regulation of glycogen synthesis by amino acids in cultured human muscle cells J Biol Chem 276 2001 952 956 (Pubitemid 32096514)
5. P.J. Atherton, J. Babraj, K. Smith, J. Singh, M.J. Rennie, and H. Wackerhage Selective activation of AMPK-PGC-1alpha or PKB-TSC2-mTOR signaling can explain specific adaptive responses to endurance or resistance training-like electrical muscle stimulation FASEB J 19 2005 786 788 (Pubitemid 40617384)
6. A. Avila-Flores, T. Santos, E. Rincon, and I. Merida Modulation of the mammalian target of rapamycin pathway by diacylglycerol kinase-produced phosphatidic acid J Biol Chem 280 2005 10091 10099 (Pubitemid 40395861)
7. J. Avruch, K. Hara, Y. Lin, M. Liu, X. Long, and S. Ortiz-Vega Insulin and amino-acid regulation of mTOR signaling and kinase activity through the Rheb GTPase Oncogene 25 2006 6361 6372 (Pubitemid 44596154)
8. J. Avruch, X. Long, S. Ortiz-Vega, J. Rapley, A. Papageorgiou, and N. Dai Amino acid regulation of TOR complex 1 Am J Physiol Endocrinol Metab 296 2009 E592 602
9. K. Baar, and K. Esser Phosphorylation of p70(S6k) correlates with increased skeletal muscle mass following resistance exercise Am J Physiol 276 1999 C120 127
10. X. Bai, D. Ma, A. Liu, X. Shen, Q.J. Wang, and Y. Liu Rheb activates mTOR by antagonizing its endogenous inhibitor, FKBP38 Science 318 2007 977 980 (Pubitemid 350098994)
11. S.C. Bodine, T.N. Stitt, M. Gonzalez, W.O. Kline, G.L. Stover, and R. Bauerlein Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo Nat Cell Biol 3 2001 1014 1019 (Pubitemid 34428747)
12. D.R. Bolster, N. Kubica, S.J. Crozier, D.L. Williamson, P.A. Farrell, and S.R. Kimball Immediate response of mammalian target of rapamycin (mTOR)-mediated signalling following acute resistance exercise in rat skeletal muscle J Physiol 553 2003 213 220 (Pubitemid 37483929)
13. E.J. Brown, P.A. Beal, C.T. Keith, J. Chen, T.B. Shin, and S.L. Schreiber Control of p70 s6 kinase by kinase activity of FRAP in vivo Nature 377 1995 441 446
14. M.D. Bruss, E.B. Arias, G.E. Lienhard, and G.D. Cartee Increased phosphorylation of Akt substrate of 160 kDa (AS160) in rat skeletal muscle in response to insulin or contractile activity Diabetes 54 2005 41 50 (Pubitemid 40105093)
15. C.J. Carlson, Z. Fan, S.E. Gordon, and F.W. Booth Time course of the MAPK and PI3-kinase response within 24 h of skeletal muscle overload J Appl Physiol 91 2001 2079 2087 (Pubitemid 33015059)
16. G.M. Carman, and G.S. Han Roles of phosphatidate phosphatase enzymes in lipid metabolism Trends Biochem Sci 31 2006 694 699 (Pubitemid 44791946)
17. Y. Chen, V. Rodrik, and D.A. Foster Alternative phospholipase D/mTOR survival signal in human breast cancer cells Oncogene 24 2005 672 679 (Pubitemid 40188571)
18. Y. Chen, Y. Zheng, and D.A. Foster Phospholipase D confers rapamycin resistance in human breast cancer cells Oncogene 22 2003 3937 3942 (Pubitemid 36819667)
19. Y.W. Chen, G.A. Nader, K.R. Baar, M.J. Fedele, E.P. Hoffman, and K.A. Esser Response of rat muscle to acute resistance exercise defined by transcriptional and translational profiling J Physiol 545 2002 27 41 (Pubitemid 35386128)
20. P.J. Cleland, G.J. Appleby, S. Rattigan, and M.G. Clark Exercise-induced translocation of protein kinase C and production of diacylglycerol and phosphatidic acid in rat skeletal muscle in vivo. Relationship to changes in glucose transport J Biol Chem 264 1989 17704 17711 (Pubitemid 19279231)
21. M. Coon, A. Ball, J. Pound, S. Ap, D. Hollenback, and T. White Inhibition of lysophosphatidic acid acyltransferase beta disrupts proliferative and survival signals in normal cells and induces apoptosis of tumor cells Mol Cancer Ther 2 2003 1067 1078
22. M.N. Corradetti, and K.L. Guan Upstream of the mammalian target of rapamycin: do all roads pass through mTOR? Oncogene 25 2006 6347 6360 (Pubitemid 44582281)
23. A. Deshmukh, V.G. Coffey, Z. Zhong, A.V. Chibalin, J.A. Hawley, and J.R. Zierath Exercise-induced phosphorylation of the novel Akt substrates AS160 and filamin A in human skeletal muscle Diabetes 55 2006 1776 1782 (Pubitemid 44324132)
24. M.J. Drummond, C.S. Fry, E.L. Glynn, H.C. Dreyer, S. Dhanani, and K.L. Timmerman Rapamycin administration in humans blocks the contraction-induced increase in skeletal muscle protein synthesis J Physiol 587 2009 1535 1546
25. M.M. Facchinetti, R. Boland, and A.R. de Boland Calcitriol transmembrane signalling: regulation of rat muscle phospholipase D activity J Lipid Res 39 1998 197 204 (Pubitemid 28063555)
26. Y. Fang, M. Vilella-Bach, R. Bachmann, A. Flanigan, and J. Chen Phosphatidic acid-mediated mitogenic activation of mTOR signaling Science 294 2001 1942 1945 (Pubitemid 33101594)
27. D.C. Fingar, C.J. Richardson, A.R. Tee, L. Cheatham, C. Tsou, and J. Blenis mTOR controls cell cycle progression through its cell growth effectors S6K1 and 4E-BP1/eukaryotic translation initiation factor 4E Mol Cell Biol 24 2004 200 216 (Pubitemid 38010048)
28. D.C. Fingar, S. Salama, C. Tsou, E. Harlow, and J. Blenis Mammalian cell size is controlled by mTOR and its downstream targets S6K1 and 4EBP1/eIF4E Genes Dev 16 2002 1472 1487 (Pubitemid 34686329)
29. R.H. Fitts, D.R. Riley, and J.J. Widrick Physiology of a microgravity environment invited review: microgravity and skeletal muscle J Appl Physiol 89 2000 823 839 (Pubitemid 30637134)
30. D.A. Foster Regulation of mTOR by phosphatidic acid? Cancer Res 67 2007 1 4 (Pubitemid 46142751)
31. R.A. Frost, and C.H. Lang Protein kinase B/Akt: a nexus of growth factor and cytokine signaling in determining muscle mass J Appl Physiol 103 2007 378 387 (Pubitemid 47092315)
32. N. Fujii, N. Jessen, and L.J. Goodyear AMP-activated protein kinase and the regulation of glucose transport Am J Physiol Endocrinol Metab 291 2006 E867 877
33. F. Gebauer, and M.W. Hentze Molecular mechanisms of translational control Nat Rev Mol Cell Biol 5 2004 827 835 (Pubitemid 39336276)
34. A.L. Goldberg Protein synthesis during work-induced growth of skeletal muscle J Cell Biol 36 1968 653 658
35. A.L. Goldberg, J.D. Etlinger, D.F. Goldspink, and C. Jablecki Mechanism of work-induced hypertrophy of skeletal muscle Med Sci Sports 7 1975 185 198
36. D.F. Goldspink The influence of immobilization and stretch on protein turnover of rat skeletal muscle J Physiol 264 1977 267 282 (Pubitemid 8029830)
37. C.A. Goodman, D.M. Mabrey, J.W. Frey, M.H. Miu, E.K. Schmidt, and P. Pierre Novel insights into the regulation of skeletal muscle protein synthesis as revealed by a new nonradioactive in vivo technique FASEB J 25 2011 1028 1039
38. C.A. Goodman, M.H. Miu, J.W. Frey, D.M. Mabrey, H.C. Lincoln, and Y. Ge 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 2010 3258 3268
39. D.A. Guertin, D.M. Stevens, C.C. Thoreen, A.A. Burds, N.Y. Kalaany, and J. Moffat Ablation in mice of the mTORC components raptor, rictor, or mLST8 reveals that mTORC2 is required for signaling to Akt-FOXO and PKCalpha, but not S6K1 Dev Cell 11 2006 859 871 (Pubitemid 44804279)
40. 2+/CaM signaling to hVps34 Cell Metab 7 2008 456 465 (Pubitemid 351598024)
41. P. Gulati, and G. Thomas Nutrient sensing in the mTOR/S6K1 signalling pathway Biochem Soc Trans 35 2007 236 238 (Pubitemid 46596477)
42. D.M. Gwinn, D.B. Shackelford, D.F. Egan, M.M. Mihaylova, A. Mery, and D.S. Vasquez AMPK phosphorylation of raptor mediates a metabolic checkpoint Mol Cell 30 2008 214 226 (Pubitemid 351626684)
43. S.H. Ha, D.H. Kim, I.S. Kim, J.H. Kim, M.N. Lee, and H.J. Lee PLD2 forms a functional complex with mTOR/raptor to transduce mitogenic signals Cell Signal 18 2006 2283 2291 (Pubitemid 44636169)
44. F. Haddad, and G.R. Adams Aging-sensitive cellular and molecular mechanisms associated with skeletal muscle hypertrophy J Appl Physiol 100 2006 1188 1203 (Pubitemid 43671476)
45. A. Hahn-Windgassen, V. Nogueira, C.C. Chen, J.E. Skeen, N. Sonenberg, and N. Hay Akt activates the mammalian target of rapamycin by regulating cellular ATP level and AMPK activity J Biol Chem 280 2005 32081 32089 (Pubitemid 41361813)
46. S. Haq, H. Kilter, A. Michael, J. Tao, E. O'Leary, and X.M. Sun Deletion of cytosolic phospholipase A2 promotes striated muscle growth Nat Med 9 2003 944 951 (Pubitemid 36889939)
47. T.E. Harris, T.A. Huffman, A. Chi, J. Shabanowitz, D.F. Hunt, and A. Kumar Insulin controls subcellular localization and multisite phosphorylation of the phosphatidic acid phosphatase, lipin 1 J Biol Chem 282 2007 277 286 (Pubitemid 47076630)
48. S.B. Hooks, S.P. Ragan, and K.R. Lynch Identification of a novel human phosphatidic acid phosphatase type 2 isoform FEBS Lett 427 1998 188 192 (Pubitemid 28225055)
49. T.A. Hornberger, and S. Chien Mechanical stimuli and nutrients regulate rapamycin-sensitive signaling through distinct mechanisms in skeletal muscle J Cell Biochem 97 2006 1207 1216
50. T.A. Hornberger, W.K. Chu, Y.W. Mak, J.W. Hsiung, S.A. Huang, and S. Chien The role of phospholipase D and phosphatidic acid in the mechanical activation of mTOR signaling in skeletal muscle Proc Natl Acad Sci USA 103 2006 4741 4746
51. T.A. Hornberger, T.J. McLoughlin, J.K. Leszczynski, D.D. Armstrong, R.R. Jameson, and P.E. Bowen Selenoprotein-deficient transgenic mice exhibit enhanced exercise-induced muscle growth J Nutr 133 2003 3091 3097 (Pubitemid 37222221)
52. T.A. Hornberger, R. Stuppard, K.E. Conley, M.J. Fedele, M.L. Fiorotto, and E.R. Chin Mechanical stimuli regulate rapamycin-sensitive signalling by a phosphoinositide 3-kinase-, protein kinase B- and growth factor-independent mechanism Biochem J 380 2004 795 804 (Pubitemid 38850521)
53. T.A. Hornberger, K.B. Sukhija, X.R. Wang, and S. Chien mTOR is the rapamycin-sensitive kinase that confers mechanically-induced phosphorylation of the hydrophobic motif site Thr(389) in p70(S6k) FEBS Lett 581 2007 4562 4566 (Pubitemid 47418781)
54. J. Huang, and B.D. Manning The TSC1-TSC2 complex: a molecular switchboard controlling cell growth Biochem J 412 2008 179 190 (Pubitemid 351758225)
55. K. Inoki, Y. Li, T. Xu, and K.L. Guan Rheb GTPase is a direct target of TSC2 GAP activity and regulates mTOR signaling Genes Dev 17 2003 1829 1834 (Pubitemid 36944560)
56. Y. Izumiya, T. Hopkins, C. Morris, K. Sato, L. Zeng, and J. Viereck Fast/glycolytic muscle fiber growth reduces fat mass and improves metabolic parameters in obese mice Cell Metab 7 2008 159 172 (Pubitemid 351168553)
57. E. Jacinto, R. Loewith, A. Schmidt, S. Lin, M.A. Ruegg, and A. Hall Mammalian TOR complex 2 controls the actin cytoskeleton and is rapamycin insensitive Nat Cell Biol 6 2004 1122 1128 (Pubitemid 39468014)
58. G.M. Jenkins, and M.A. Frohman Phospholipase D: a lipid centric review Cell Mol Life Sci 62 2005 2305 2316 (Pubitemid 41500546)
59. G. Juhasz, J.H. Hill, Y. Yan, M. Sass, E.H. Baehrecke, and J.M. Backer The class III PI(3)K Vps34 promotes autophagy and endocytosis but not TOR signaling in Drosophila J Cell Biol 181 2008 655 666 (Pubitemid 351717512)
60. 2+-independent phosphatidic acid phosphatase J Biol Chem 272 1997 24572 24578 (Pubitemid 27418671)
61. K. Katayama, T. Kodaki, Y. Nagamachi, and S. Yamashita Cloning, differential regulation and tissue distribution of alternatively spliced isoforms of ADP-ribosylation-factor-dependent phospholipase D from rat liver Biochem J 329 Pt 3 1998 647 652 (Pubitemid 28055189)
62. E. Kim, P. Goraksha-Hicks, L. Li, T.P. Neufeld, and K.L. Guan Regulation of TORC1 by Rag GTPases in nutrient response Nat Cell Biol 10 2008 935 945
63. E. Kim, and K.L. Guan RAG GTPases in nutrient-mediated TOR signaling pathway Cell Cycle 8 2009 1014 1018
64. J. Kim, R.S. Solis, E.B. Arias, and G.D. Cartee Postcontraction insulin sensitivity: relationship with contraction protocol, glycogen concentration, and 5′ AMP-activated protein kinase phosphorylation J Appl Physiol 96 2004 575 583 (Pubitemid 38140159)
65. S.R. Kimball Interaction between the AMP-activated protein kinase and mTOR signaling pathways Med Sci Sports Exerc 38 2006 1958 1964 (Pubitemid 44707801)
66. S.R. Kimball, P.A. Farrell, and L.S. Jefferson Invited Review: role of insulin in translational control of protein synthesis in skeletal muscle by amino acids or exercise J Appl Physiol 93 2002 1168 1180 (Pubitemid 34919691)
67. S.R. Kimball, L.M. Shantz, R.L. Horetsky, and L.S. Jefferson 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 274 1999 11647 11652
68. T. Kodaki, and S. Yamashita Cloning, expression, and characterization of a novel phospholipase D complementary DNA from rat brain J Biol Chem 272 1997 11408 11413 (Pubitemid 27184146)
69. N. Kubica, D.R. Bolster, P.A. Farrell, S.R. Kimball, and L.S. Jefferson 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 2004
70. N. Kubica, D.R. Bolster, P.A. Farrell, S.R. Kimball, and L.S. Jefferson 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 2005 7570 7580 (Pubitemid 40349649)
71. H.A. Lane, A. Fernandez, N.J. Lamb, and G. Thomas p70s6k function is essential for G1 progression Nature 363 1993 170 172
72. R.C. Lee, Z. Wang, M. Heo, R. Ross, I. Janssen, and S.B. Heymsfield Total-body skeletal muscle mass: development and cross-validation of anthropometric prediction models Am J Clin Nutr 72 2000 796 803
73. N.C. Lockhart, K. Baar, R.S. Mazzeo, and S.V. Brooks Activation of Akt as a potential mediator of adaptations that reduce muscle injury Med Sci Sports Exerc 38 2006 1058 1064 (Pubitemid 43902486)
74. X. Long, S. Ortiz-Vega, Y. Lin, and J. Avruch Rheb binding to mammalian target of rapamycin (mTOR) is regulated by amino acid sufficiency J Biol Chem 280 2005 23433 23436 (Pubitemid 40884818)
75. M.C. Lorenz, and J. Heitman TOR mutations confer rapamycin resistance by preventing interaction with FKBP12-rapamycin J Biol Chem 270 1995 27531 27537
76. B. Lu, Y.J. Jiang, Y. Zhou, F.Y. Xu, G.M. Hatch, and P.C. Choy Cloning and characterization of murine 1-acyl-sn-glycerol 3-phosphate acyltransferases and their regulation by PPARalpha in murine heart Biochem J 385 2005 469 477 (Pubitemid 40165080)
77. D. Ma, X. Bai, S. Guo, and Y. Jiang The switch I region of Rheb is critical for its interaction with FKBP38 J Biol Chem 283 2008 25963 25970
78. M.G. MacKenzie, D.L. Hamilton, J.T. Murray, P.M. Taylor, and K. Baar mVps34 is activated following high-resistance contractions J Physiol 587 2009 253 260
79. S.J. Mahoney, J.M. Dempsey, and J. Blenis Cell signaling in protein synthesis ribosome biogenesis and translation initiation and elongation Prog Mol Biol Transl Sci 90C 2009 53 107 [Chapter 2]
80. O. Meyuhas Synthesis of the translational apparatus is regulated at the translational level Eur J Biochem 267 2000 6321 6330
81. M. Murakami, and I. Kudo Phospholipase A2 J Biochem 131 2002 285 292
82. N. Musi, H. Yu, and L.J. Goodyear AMP-activated protein kinase regulation and action in skeletal muscle during exercise Biochem Soc Trans 31 2003 191 195 (Pubitemid 36241426)
83. G.A. Nader Molecular determinants of skeletal muscle mass: getting the "AKT" together Int J Biochem Cell Biol 37 2005 1985 1996 (Pubitemid 41206816)
84. M. Nanjundan, and F. Possmayer Pulmonary phosphatidic acid phosphatase and lipid phosphate phosphohydrolase Am J Physiol Lung Cell Mol Physiol 284 2003 L1 23
85. T. Nobukuni, M. Joaquin, M. Roccio, S.G. Dann, S.Y. Kim, and P. Gulati Amino acids mediate mTOR/raptor signaling through activation of class 3 phosphatidylinositol 3OH-kinase Proc Natl Acad Sci USA 102 2005 14238 14243 (Pubitemid 41429682)
86. T.K. O'Neil, L.R. Duffy, J.W. Frey, and T.A. Hornberger The role of phosphoinositide 3-kinase and phosphatidic acid in the regulation of mTOR following eccentric contractions J Physiol 587 2009 3691 3701
87. M. Ohanna, A.K. Sobering, T. Lapointe, L. Lorenzo, C. Praud, and E. Petroulakis Atrophy of S6K1(-/-) skeletal muscle cells reveals distinct mTOR effectors for cell cycle and size control Nat Cell Biol 7 2005 286 294 (Pubitemid 40331130)
88. P.A. Oude Weernink, L. Han, K.H. Jakobs, and M. Schmidt Dynamic phospholipid signaling by G protein-coupled receptors Biochim Biophys Acta 1768 2007 888 900 (Pubitemid 46452539)
89. M. Pahor, and S. Kritchevsky Research hypotheses on muscle wasting, aging, loss of function and disability J Nutr Health Aging 2 1998 97 100 (Pubitemid 128695283)
90. G. Pallafacchina, E. Calabria, A.L. Serrano, J.M. Kalhovde, and S. Schiaffino A protein kinase B-dependent and rapamycin-sensitive pathway controls skeletal muscle growth but not fiber type specification Proc Natl Acad Sci USA 99 2002 9213 9218 (Pubitemid 34764593)
91. M. Pende, S.H. Um, V. Mieulet, M. Sticker, V.L. Goss, and J. Mestan S6K1(-/-)/S6K2(-/-) mice exhibit perinatal lethality and rapamycin-sensitive 5′-terminal oligopyrimidine mRNA translation and reveal a mitogen-activated protein kinase-dependent S6 kinase pathway Mol Cell Biol 24 2004 3112 3124 (Pubitemid 38452057)
92. D.N. Proctor, P. Balagopal, and K.S. Nair Age-related sarcopenia in humans is associated with reduced synthetic rates of specific muscle proteins J Nutr 128 1998 351S 355S (Pubitemid 28090378)
93. C.G. Proud Signalling to translation: how signal transduction pathways control the protein synthetic machinery Biochem J 403 2007 217 234 (Pubitemid 46596577)
94. J.H. Reiling, and D.M. Sabatini Stress and mTORture signaling Oncogene 25 2006 6373 6383 (Pubitemid 44582282)
95. C. Rommel, S.C. Bodine, B.A. Clarke, R. Rossman, L. Nunez, and T.N. Stitt Mediation of IGF-1-induced skeletal myotube hypertrophy by PI(3)K/Akt/mTOR and PI(3)K/Akt/GSK3 pathways Nat Cell Biol 3 2001 1009 1013 (Pubitemid 34428746)
96. K. Sakamoto, W.G. Aschenbach, M.F. Hirshman, and L.J. Goodyear Akt signaling in skeletal muscle: regulation by exercise and passive stretch Am J Physiol Endocrinol Metab 285 2003 E1081 1088
97. F. Sakane, S. Imai, M. Kai, S. Yasuda, and H. Kanoh Diacylglycerol kinases: why so many of them? Biochim Biophys Acta 1771 2007 793 806 (Pubitemid 46891299)
98. Y. Sancak, L. Bar-Peled, R. Zoncu, A.L. Markhard, S. Nada, and D.M. Sabatini Ragulator-Rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids Cell 141 2010 290 303
99. Y. Sancak, T.R. Peterson, Y.D. Shaul, R.A. Lindquist, C.C. Thoreen, and L. Bar-Peled The Rag GTPases bind raptor and mediate amino acid signaling to mTORC1 Science 320 2008 1496 1501 (Pubitemid 351929429)
100. M. Sandri Signaling in muscle atrophy and hypertrophy Physiology (Bethesda) 23 2008 160 170
101. R. Seguin, and M.E. Nelson The benefits of strength training for older adults Am J Prev Med 25 2003 141 149 (Pubitemid 41116508)
102. Y. Shen, L. Xu, and D.A. Foster Role for phospholipase D in receptor-mediated endocytosis Mol Cell Biol 21 2001 595 602 (Pubitemid 32037377)
103. H. Shima, M. Pende, Y. Chen, S. Fumagalli, G. Thomas, and S.C. Kozma Disruption of the p70(s6k)/p85(s6k) gene reveals a small mouse phenotype and a new functional S6 kinase EMBO J 17 1998 6649 6659 (Pubitemid 28521798)
104. E.E. Spangenburg, D. Le Roith, C.W. Ward, and S.C. Bodine A functional insulin-like growth factor receptor is not necessary for load-induced skeletal muscle hypertrophy J Physiol 586 2008 283 291
105. E.E. Spangenburg, and T.A. McBride Inhibition of stretch-activated channels during eccentric muscle contraction attenuates p70S6K activation J Appl Physiol 100 2006 129 135 (Pubitemid 43671099)
106. W. Su, O. Yeku, S. Olepu, A. Genna, J.S. Park, and H. Ren 5-Fluoro-2-indolyl des-chlorohalopemide (FIPI), a phospholipase D pharmacological inhibitor that alters cell spreading and inhibits chemotaxis Mol Pharmacol 75 2009 437 446
107. Y. Sun, Y. Fang, M.S. Yoon, C. Zhang, M. Roccio, and F.J. Zwartkruis Phospholipase D1 is an effector of Rheb in the mTOR pathway Proc Natl Acad Sci USA 105 2008 8286 8291 (Pubitemid 351904748)
108. N. Takahashi, M. Nagamine, S. Tanno, W. Motomura, Y. Kohgo, and T. Okumura A diacylglycerol kinase inhibitor, R59022, stimulates glucose transport through a MKK3/6-p38 signaling pathway in skeletal muscle cells Biochem Biophys Res Commun 360 2007 244 250 (Pubitemid 46990350)
109. W. Tang, J. Yuan, X. Chen, X. Gu, K. Luo, and J. Li Identification of a novel human lysophosphatidic acid acyltransferase, LPAAT-theta, which activates mTOR pathway J Biochem Mol Biol 39 2006 626 635 (Pubitemid 44714544)
110. M.K. Topham Signaling roles of diacylglycerol kinases J Cell Biochem 97 2006 474 484 (Pubitemid 43265307)
111. H.H. Vandenburgh, S. Hatfaludy, I. Sohar, and J. Shansky Stretch-induced prostaglandins and protein turnover in cultured skeletal muscle Am J Physiol 259 1990 C232 C240
112. H. Vandenburgh, J. Chromiak, J. Shansky, M. Del Tatto, and J. Lemaire Space travel directly induces skeletal muscle atrophy FASEB J 13 1999 1031 1038 (Pubitemid 29249728)
113. H.H. Vandenburgh Motion into mass: how does tension stimulate muscle growth? Med Sci Sports Exerc 19 1987 S142 149
114. H.H. Vandenburgh, and S. Kaufman Stretch-induced growth of skeletal myotubes correlates with activation of the sodium pump J Cell Physiol 109 1981 205 214 (Pubitemid 12228518)
115. S. Varma, and R.L. Khandelwal Effects of rapamycin on cell proliferation and phosphorylation of mTOR and p70(S6K) in HepG2 and HepG2 cells overexpressing constitutively active Akt/PKB Biochim Biophys Acta 1770 2007 71 78 (Pubitemid 44909343)
116. V. Veverka, T. Crabbe, I. Bird, G. Lennie, F.W. Muskett, and R.J. Taylor Structural characterization of the interaction of mTOR with phosphatidic acid and a novel class of inhibitor: compelling evidence for a central role of the FRB domain in small molecule-mediated regulation of mTOR Oncogene 27 2008 585 595 (Pubitemid 351158903)
117. M.J. Wakelam, M. Hodgkin, and A. Martin The measurement of phospholipase D-linked signaling in cells Methods Mol Biol 41 1995 271 278
118. X. Wang, S.P. Devaiah, W. Zhang, and R. Welti Signaling functions of phosphatidic acid Prog Lipid Res. 2006
119. J.N. Winter, T.E. Fox, M. Kester, L.S. Jefferson, and S.R. Kimball Phosphatidic acid mediates activation of mTORC1 through the ERK signaling pathway Am J Physiol Cell Physiol 299 2010 C335 C344
120. 2+/CaM, is required for the activity and regulation of hVps34 in mammalian cells Biochem J 417 2009 747 755
121. Q. Yang, and K.L. Guan Expanding mTOR signaling Cell Res 17 2007 666 681 (Pubitemid 47255937)