Focal adhesion kinase is required for IGF-I-mediated growth of skeletal muscle cells via a TSC2/mTOR/S6K1-associated pathway

American Journal of Physiology - Endocrinology and Metabolism

Volumn 305, Issue 2, 2013, Pages

  Crossland, Hannah ^a,c   Kazi, Abid A ^b   Lang, Charles H ^b   Timmons, James A ^c   Pierre, Philippe ^d,e,f   Wilkinson, Daniel J ^a   Smith, Kenneth ^a   Szewczyk, Nathaniel J ^a   Atherton, Philip J ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b PENN STATE COLLEGE OF MEDICINE   (United States)

^c LOUGHBOROUGH UNIVERSITY   (United Kingdom)

^d CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^e INSERM   (France)

^f CNRS   (France)

Author keywords

Focal adhesion kinase; Hypertrophy; Insulin like growth factor I; Mammalian target of rapamycin; S6 kinase 1; Skeletal muscle; Tuberous sclerosis complex 2

Indexed keywords

FOCAL ADHESION KINASE; INITIATION FACTOR 4F; MAMMALIAN TARGET OF RAPAMYCIN; MUSCLE PROTEIN; PROTEIN TYROSINE PHOSPHATASE SHP 2; S6 KINASE; SHORT HAIRPIN RNA; SOMATOMEDIN C; TUBERIN;

ANIMAL CELL; ARTICLE; CELL GROWTH; CHROMATIN IMMUNOPRECIPITATION; IMMUNOBLOTTING; MOUSE; MUSCLE HYPERTROPHY; MYOTUBE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; SKELETAL MUSCLE; SYNTHESIS;

FOCAL ADHESION KINASE; HYPERTROPHY; INSULIN-LIKE GROWTH FACTOR-I; MAMMALIAN TARGET OF RAPAMYCIN; S6 KINASE 1; SKELETAL MUSCLE; TUBEROUS SCLEROSIS COMPLEX 2;

ALGORITHMS; ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; FOCAL ADHESION PROTEIN-TYROSINE KINASES; GENETIC VECTORS; IMMUNOPRECIPITATION; INSULIN-LIKE GROWTH FACTOR I; LENTIVIRUS; MICE; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; PHOSPHORYLATION; RIBOSOMAL PROTEIN S6 KINASES, 90-KDA; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; TUMOR SUPPRESSOR PROTEINS;

EID: 84880171279     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00541.2012     Document Type: Article

References (60)

1. Alessi DR, Andjelkovic M, Caudwell B, Cron P, Morrice N, Cohen P, Hemmings BA. Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO J 15: 6541-6551, 1996.
2. Andersson S, D'Arcy P, Larsson O, Sehat B. Focal adhesion kinase (FAK) activates and stabilizes IGF-1 receptor. Biochem Biophys Res Commun 387: 36-41, 2009.
3. Baron V, Calleja V, Ferrari P, Alengrin F, Van Obberghen E. p125Fak focal adhesion kinase is a substrate for the insulin and insulinlike growth factor-I tyrosine kinase receptors. J Biol Chem 273: 7162-7168, 1998.
4. Bentzinger CF, Lin S, Romanino K, Castets P, Guridi M, Summermatter S, Handschin C, Tintignac LA, Hall MN, Rüegg MA. Differential response of skeletal muscles to mTORC1 signaling during atrophy and hypertrophy. Skelet Muscle 3: 6, 2013.
5. 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.
6. Brunn GJ, Hudson CC, Sekulíc A, Williams JM, Hosoi H, Houghton PJ, Lawrence JC Jr, Abraham RT. Phosphorylation of the translational repressor PHAS-I by the mammalian target of rapamycin. Science 277: 99-101, 1997.
7. Burridge K, Chrzanowska-Wodnicka M Focal adhesions, contractility, and signaling. Annu Rev Cell Dev Biol 12: 463-518, 1996.
8. Calalb MB, Polte TR, Hanks SK. Tyrosine phosphorylation of focal adhesion kinase at sites in the catalytic domain regulates kinase activity: a role for Src family kinases. Mol Cell Biol 15: 954-963, 1995.
9. Cary LA, Guan JL. Focal adhesion kinase in integrin-mediated signaling. Front Biosci 4: D102-D113, 1999.
10. Casamassima A, Rozengurt E. Insulin-like growth factor I stimulates tyrosine phosphorylation of p130(Cas), focal adhesion kinase, and paxillin. Role of phosphatidylinositol 3-kinase and formation of a p130(Cas) Crk complex. J Biol Chem 273: 26149-26156, 1998.
11. Clemente CF, Xavier-Neto J, Dalla Costa AP, Consonni SR, Antunes JE, Rocco SA, Pereira MB, Judice CC, Strauss B, Joazeiro PP, Matos-Souza JR, Franchini KG. Focal adhesion kinase governs cardiac concentric hypertrophic growth by activating the AKT and mTOR pathways. J Mol Cell Cardiol 52: 493-501, 2012.
12. Conti FJ, Felder A, Monkley S, Schwander M, Wood MR, Lieber R, Critchley D, Muller U. Progressive myopathy and defects in the maintenance of myotendinous junctions in mice that lack talin 1 in skeletal muscle. Development 135: 2043-2053, 2008.
13. de Boer MD, Selby A, Atherton P, Smith K, Seynnes OR, Maganaris CN, Maffulli N, Movin T, Narici MV, Rennie MJ. The temporal responses of protein synthesis, gene expression and cell signalling in human quadriceps muscle and patellar tendon to disuse. J Physiol 585: 241-251, 2007.
14. de Oliveira MV, Marin TM, Clemente CF, Costa AP, Judice CC, Franchini KG. SHP-2 regulates myogenesis by coupling to FAK signaling pathway. FEBS Lett 583: 2975-2981, 2009.
15. Domingos PP, Fonseca PM, Nadruz W Jr, Franchini KG. Loadinduced focal adhesion kinase activation in the myocardium: role of stretch and contractile activity. Am J Physiol Heart Circ Physiol 282: H556-H564, 2002.
16. Durieux AC, D'Antona G, Desplanches D, Freyssenet D, Klossner S, Bottinelli R, Fluck M. Focal adhesion kinase is a load-dependent governor of the slow contractile and oxidative muscle phenotype. J Physiol 587: 3703-3717, 2009.
17. Etheridge T, Oczypok EA, Lehmann S, Fields BD, Shephard F, Jacobson LA, Szewczyk NJ. Calpains mediate integrin attachment complex maintenance of adult muscle in Caenorhabditis elegans. PLoS Genet 8: e1002471, 2012.
18. Fluck M, Carson JA, Gordon SE, Ziemiecki A, Booth FW. Focal adhesion proteins FAK and paxillin increase in hypertrophied skeletal muscle. Am J Physiol Cell Physiol 277: C152-C162, 1999.
19. Franchini KG, Torsoni AS, Soares PH, Saad MJ. Early activation of the multicomponent signaling complex associated with focal adhesion kinase induced by pressure overload in the rat heart. Circ Res 87: 558-565, 2000.
20. Gan B, Yoo Y, Guan JL. Association of focal adhesion kinase with tuberous sclerosis complex 2 in the regulation of s6 kinase activation and cell growth. J Biol Chem 281: 37321-37329, 2006.
21. Gao X, Zhang Y, Arrazola P, Hino O, Kobayashi T, Yeung RS, Ru B, Pan D. Tsc tumour suppressor proteins antagonize amino-acid-TOR signalling. Nat Cell Biol 4: 699-704, 2002.
22. Gasier HG, Fluckey JD, Previs SF. The application of 2H2O to measure skeletal muscle protein synthesis. Nutr Metab (Lond) 7: 31, 2010.
23. Gheyara AL, Vallejo-Illarramendi A, Zang K, Mei L, St-Arnaud R, Dedhar S, Reichardt LF. Deletion of integrin-linked kinase from skeletal muscles of mice resembles muscular dystrophy due to alpha 7 beta 1-integrin deficiency. Am J Pathol 171: 1966-1977, 2007.
24. 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 586: 6049-6061, 2008.
25. Goel HL, Dey CS. Focal adhesion kinase tyrosine phosphorylation is associated with myogenesis and modulated by insulin. Cell Prolif 35: 131-142, 2002.
26. Golubovskaya VM, Nyberg C, Zheng M, Kweh F, Magis A, Ostrov D, Cance WG. A small molecule inhibitor, 1,2,4,5-benzenetetraamine tetrahydrochloride, targeting the y397 site of focal adhesion kinase decreases tumor growth. J Med Chem 51: 7405-7416, 2008.
27. Goodman CA, Mabrey DM, Frey JW, Miu MH, Schmidt EK, Pierre P, Hornberger TA. Novel insights into the regulation of skeletal muscle protein synthesis as revealed by a new nonradioactive in vivo technique. FASEB J 25: 1028-1039, 2011.
28. Gordon SE, Flück M, Booth FW. Selected Contribution: Skeletal muscle focal adhesion kinase, paxillin, and serum response factor are loading dependent. J Appl Physiol 90: 1174-1183; discussion 1165, 2001.
29. Guertin DA, Stevens DM, Thoreen CC, Burds AA, Kalaany NY, Moffat J, Brown M, Fitzgerald KJ, Sabatini DM. 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: 859-871, 2006.
30. Hynes RO. Cell adhesion: old and new questions. Trends Cell Biol 9: M33-M37, 1999.
31. Inoki K, Li Y, Zhu T, Wu J, Guan KL. TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling. Nat Cell Biol 4: 648-657, 2002.
32. Isotani S, Hara K, Tokunaga C, Inoue H, Avruch J, Yonezawa K. Immunopurified mammalian target of rapamycin phosphorylates and activates p70 S6 kinase alpha in vitro. J Biol Chem 274: 34493-34498, 1999.
33. Jacinto E, Facchinetti V, Liu D, Soto N, Wei S, Jung SY, Huang Q, Qin J, Su B. SIN1/MIP1 maintains rictor-mTOR complex integrity and regulates Akt phosphorylation and substrate specificity. Cell 127: 125-137, 2006.
34. Juliano RL. Signal transduction by cell adhesion receptors and the cytoskeleton: functions of integrins, cadherins, selectins, and immunoglobulin-superfamily members. Annu Rev Pharmacol Toxicol 42: 283-323, 2002.
35. Kazi AA, Lang CH. PRAS40 regulates protein synthesis and cell cycle in C2C12 myoblasts. Mol Med 16: 359-371, 2010.
36. Kimball SR, Shantz LM, Horetsky RL, Jefferson LS. 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: 11647-11652, 1999.
37. Klossner S, Durieux AC, Freyssenet D, Flueck M. Mechano-transduction to muscle protein synthesis is modulated by FAK. Eur J Appl Physiol 106: 389-398, 2009.
38. Kumar V, Selby A, Rankin D, Patel R, Atherton P, Hildebrandt W, Williams J, Smith K, Seynnes O, Hiscock N, Rennie MJ. Age-related differences in the dose-response relationship of muscle protein synthesis to resistance exercise in young and old men. J Physiol 587: 211-217, 2009.
39. Latres E, Amini AR, Amini AA, Griffiths J, Martin FJ, Wei Y, Lin HC, Yancopoulos GD, Glass DJ. Insulin-like growth factor-1 (IGF-1) inversely regulates atrophy-induced genes via the phosphatidylinositol 3-kinase/Akt/mammalian target of rapamycin (PI3K/Akt/mTOR) pathway. J Biol Chem 280: 2737-2744, 2005.
40. Marin TM, Clemente CF, Santos AM, Picardi PK, Pascoal VD, Lopes-Cendes I, Saad MJ, Franchini KG. Shp2 negatively regulates growth in cardiomyocytes by controlling focal adhesion kinase/Src and mTOR pathways. Circ Res 103: 813-824, 2008.
41. Monti RJ, Roy RR, Hodgson JA, Edgerton VR. Transmission of forces within mammalian skeletal muscles. J Biomech 32: 371-380, 1999.
42. Pain VM. Initiation of protein synthesis in eukaryotic cells. Eur J Biochem 236: 747-771, 1996.
43. Park IH, Erbay E, Nuzzi P, Chen J. Skeletal myocyte hypertrophy requires mTOR kinase activity and S6K1. Exp Cell Res 309: 211-219, 2005.
44. Perkins AD, Ellis SJ, Asghari P, Shamsian A, Moore ED, Tanentzapf G. Integrin-mediated adhesion maintains sarcomeric integrity. Dev Biol 338: 15-27, 2010.
45. Phillips BE, Williams JP, Gustafsson T, Bouchard C, Rankinen T, Knudsen S, Smith K, Timmons JA, Atherton PJ. Molecular networks of human muscle adaptation to exercise and age. PLoS Genet 9: e1003389, 2013.
46. Pullen N, Thomas G. The modular phosphorylation and activation of p70s6k. FEBS Lett 410: 78-82, 1997.
47. Raught B, Peiretti F, Gingras AC, Livingstone M, Shahbazian D, Mayeur GL, Polakiewicz RD, Sonenberg N, Hershey JW. Phosphorylation of eucaryotic translation initiation factor 4B Ser422 is modulated by S6 kinases. EMBO J 23: 1761-1769, 2004.
48. Rommel C, Bodine SC, Clarke BA, Rossman R, Nunez L, Stitt TN, Yancopoulos GD, Glass DJ. 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: 1009-1013, 2001.
49. Sancak Y, Thoreen CC, Peterson TR, Lindquist RA, Kang SA, Spooner E, Carr SA, Sabatini DM. PRAS40 is an insulin-regulated inhibitor of the mTORC1 protein kinase. Mol Cell 25: 903-915, 2007.
50. Sarbassov DD, Guertin DA, Ali SM, Sabatini DM. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 307: 1098-1101, 2005.
51. Schlaepfer DD, Hauck CR, Sieg DJ. Signaling through focal adhesion kinase. Prog Biophys Mol Biol 71: 435-478, 1999.
52. Schmidt EK, Clavarino G, Ceppi M, Pierre P. SUnSET, a nonradioactive method to monitor protein synthesis. Nat Methods 6: 275-277, 2009.
53. Taverna D, Disatnik MH, Rayburn H, Bronson RT, Yang J, Rando TA, Hynes RO. Dystrophic muscle in mice chimeric for expression of alpha5 integrin. J Cell Biol 143: 849-859, 1998.
54. Wan X, Harkavy B, Shen N, Grohar P, Helman LJ. Rapamycin induces feedback activation of Akt signaling through an IGF-1R-dependent mechanism. Oncogene 26: 1932-1940, 2007.
55. Wang HV, Chang LW, Brixius K, Wickstrom SA, Montanez E, Thievessen I, Schwander M, Muller U, Bloch W, Mayer U, Fassler R. Integrin-linked kinase stabilizes myotendinous junctions and protects muscle from stress-induced damage. J Cell Biol 180: 1037-1049, 2008.
56. Wang X, Li W, Williams M, Terada N, Alessi DR, Proud CG. Regulation of elongation factor 2 kinase by p90(RSK1) and p70 S6 kinase. EMBO J 20: 4370-4379, 2001.
57. Welinder C, Ekblad L. Coomassie staining as loading control in Western blot analysis. J Proteome Res 10: 1416-1419, 2011.
58. Wilkinson SB, Phillips SM, Atherton PJ, Patel R, Yarasheski KE, Tarnopolsky MA, Rennie MJ. Differential effects of resistance and endurance exercise in the fed state on signalling molecule phosphorylation and protein synthesis in human muscle. J Physiol 586: 3701-3717, 2008.
59. Yang D, Diraison F, Beylot M, Brunengraber DZ, Samols MA, Anderson VE, Brunengraber H. Assay of low deuterium enrichment of water by isotopic exchange with [U-13C3]acetone and gas chromatography-mass spectrometry. Anal Biochem 258: 315-321, 1998.
60. Zhang Y, Gao X, Saucedo LJ, Ru B, Edgar BA, Pan D. Rheb is a direct target of the tuberous sclerosis tumour suppressor proteins. Nat Cell Biol 5: 578-581, 2003.